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Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Review Article

Bone Marrow Niches for Skeletal Progenitor Cells and their Inhabitants in Health and Disease

Author(s): Marietta Herrmann* and Franz Jakob

Volume 14, Issue 4, 2019

Page: [305 - 319] Pages: 15

DOI: 10.2174/1574888X14666190123161447

Price: $65

Abstract

The bone marrow hosts skeletal progenitor cells which have most widely been referred to as Mesenchymal Stem or Stromal Cells (MSCs), a heterogeneous population of adult stem cells possessing the potential for self-renewal and multilineage differentiation. A consensus agreement on minimal criteria has been suggested to define MSCs in vitro, including adhesion to plastic, expression of typical surface markers and the ability to differentiate towards the adipogenic, osteogenic and chondrogenic lineages but they are critically discussed since the differentiation capability of cells could not always be confirmed by stringent assays in vivo. However, these in vitro characteristics have led to the notion that progenitor cell populations, similar to MSCs in bone marrow, reside in various tissues. MSCs are in the focus of numerous (pre)clinical studies on tissue regeneration and repair.

Recent advances in terms of genetic animal models enabled a couple of studies targeting skeletal progenitor cells in vivo. Accordingly, different skeletal progenitor cell populations could be identified by the expression of surface markers including nestin and leptin receptor. While there are still issues with the identity of, and the overlap between different cell populations, these studies suggested that specific microenvironments, referred to as niches, host and maintain skeletal progenitor cells in the bone marrow. Dynamic mutual interactions through biological and physical cues between niche constituting cells and niche inhabitants control dormancy, symmetric and asymmetric cell division and lineage commitment. Niche constituting cells, inhabitant cells and their extracellular matrix are subject to influences of aging and disease e.g. via cellular modulators. Protective niches can be hijacked and abused by metastasizing tumor cells, and may even be adapted via mutual education. Here, we summarize the current knowledge on bone marrow skeletal progenitor cell niches in physiology and pathophysiology. We discuss the plasticity and dynamics of bone marrow niches as well as future perspectives of targeting niches for therapeutic strategies.

Keywords: Niche, MSC, skeletal stem/progenitor cells, multiple myeloma, homing, mobilization.

[1]
Friedenstein A, Piatetzky-Shapiro I, Petrakova K. Osteogenesis in transplants of bone marrow cells. Development 1966; 16(3): 381-90.
[2]
Ireland H, Gay MHP, Baldomero H, et al. The survey on cellular and tissue-engineered therapies in Europe and neighboring Eurasian countries in 2014 and 2015. Cytotherapy 2018; 20(1): 1-20.
[3]
Caplan AI. Mesenchymal stem cells: Time to change the name! Stem Cells Transl Med 2017; 6(6): 1445-51.
[4]
Robey P. “Mesenchymal stem cells”: Fact or fiction, and implications in their therapeutic use. F1000 Res 2017; 6.
[5]
Samsonraj RM, Raghunath M, Nurcombe V, Hui JH, van Wijnen AJ, Cool SM. Concise Review: Multifaceted characterization of human mesenchymal stem cells for use in regenerative medicine. Stem Cells Transl Med 2017; 6(12): 2173-85.
[6]
Bernardo ME, Fibbe WE. Mesenchymal stromal cells: Sensors and switchers of inflammation. Cell Stem Cell 2013; 13(4): 392-402.
[7]
Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
[8]
Prager P, Kunz M, Ebert R, et al. Mesenchymal stem cells isolated from the anterior cruciate ligament: Characterization and comparison of cells from young and old donors. Knee Surg Relat Res 2018; 30(3): 193-205.
[9]
Steinert AF, Kunz M, Prager P, et al. Characterization of bursa subacromialis-derived mesenchymal stem cells. Stem Cell Res Ther 2015; 6: 114.
[10]
Limbert C, Path G, Ebert R, et al. PDX1- and NGN3-mediated in vitro reprogramming of human bone marrow-derived mesenchymal stromal cells into pancreatic endocrine lineages. Cytotherapy 2011; 13(7): 802-13.
[11]
Sacchetti B, Funari A, Remoli C, et al. No identical “mesenchymal stem cells” at different times and sites: human committed progenitors of distinct origin and differentiation potential are incorporated as adventitial cells in microvessels. Stem Cell Reports 2016; 6(6): 897-913.
[12]
Caplan AI. New MSC: MSCs as pericytes are Sentinels and gatekeepers. J Orthop Res 2017; 35(6): 1151-9.
[13]
Chen KG, Johnson KR, McKay RDG, Robey PG. Concise eview: Conceptualizing paralogous stem-cell niches and unfolding bone marrow progenitor cell identities. Stem Cells 2018; 36(1): 11-21.
[14]
Hall BK. Germ layers, the neural crest and emergent organization in development and evolution. Genesis 2018; 56(6-7): e23103.
[15]
Slukvin II, Kumar A. The mesenchymoangioblast, mesodermal precursor for mesenchymal and endothelial cells. Cell Mol Life Sci 2018; 75(19): 3507-20.
[16]
Kuratani S. The neural crest and origin of the neurocranium in vertebrates. Genesis 2018; 56(6-7): e23213.
[17]
Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978; 4(1-2): 7-25.
[18]
Gonzalez-Reyes A. Stem cells, niches and cadherins: A view from Drosophila. J Cell Sci 2003; 116(Pt 6): 949-54.
[19]
Tanaka EM. The molecular and cellular choreography of appendage regeneration. Cell 2016; 165(7): 1598-608.
[20]
Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3(3): 301-13.
[21]
Guimaraes-Camboa N, Cattaneo P, Sun Y, et al. Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell 2017; 20(3): 345-59 e5.
[22]
Nombela-Arrieta C, Pivarnik G, Winkel B, et al. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol 2013; 15(5): 533-43.
[23]
Crane GM, Jeffery E, Morrison SJ. Adult haematopoietic stem cell niches. Nat Rev Immunol 2017; 17(9): 573-90.
[24]
Asada N, Kunisaki Y, Pierce H, et al. Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat Cell Biol 2017; 19(3): 214-23.
[25]
Ehninger A, Trumpp A. The bone marrow stem cell niche grows up: Mesenchymal stem cells and macrophages move in. J Exp Med 2011; 208(3): 421-8.
[26]
Katayama Y, Battista M, Kao WM, et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006; 124(2): 407-21.
[27]
Schepers K, Campbell TB, Passegue E. Normal and leukemic stem cell niches: Insights and therapeutic opportunities. Cell Stem Cell 2015; 16(3): 254-67.
[28]
Chan CK, Chen CC, Luppen CA, et al. Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 2009; 457(7228): 490-4.
[29]
Morikawa S, Mabuchi Y, Kubota Y, et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 2009; 206(11): 2483-96.
[30]
Pinho S, Lacombe J, Hanoun M, et al. PDGFRalpha and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J Exp Med 2013; 210(7): 1351-67.
[31]
Nakamura Y, Arai F, Iwasaki H, et al. Isolation and characterization of endosteal niche cell populations that regulate hematopoietic stem cells. Blood 2010; 116(9): 1422-32.
[32]
Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006; 25(6): 977-88.
[33]
Omatsu Y, Sugiyama T, Kohara H, et al. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 2010; 33(3): 387-99.
[34]
Méndez-Ferrer S, Michurina TV, Ferraro F, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010; 466(7308): 829.
[35]
Zhou BO, Yue R, Murphy MM, Peyer JG, Morrison SJ. Leptin-receptor-expressing mesenchymal stromal cells represent the main source of bone formed by adult bone marrow. Cell Stem Cell 2014; 15(2): 154-68.
[36]
Mizoguchi T, Pinho S, Ahmed J, et al. Osterix marks distinct waves of primitive and definitive stromal progenitors during bone marrow development. Dev Cell 2014; 29(3): 340-9.
[37]
Worthley DL, Churchill M, Compton JT, et al. Gremlin 1 identifies a skeletal stem cell with bone, cartilage, and reticular stromal potential. Cell 2015; 160(1-2): 269-84.
[38]
Kramann R, Schneider RK, DiRocco DP, et al. Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 2015; 16(1): 51-66.
[39]
Schneider RK, Mullally A, Dugourd A, et al. Gli1(+) mesenchymal stromal cells are a key driver of bone marrow fibrosis and an important cellular therapeutic target. Cell Stem Cell 2017; 20(6): 785- 800 e8.
[40]
Lv FJ, Tuan RS, Cheung KM, Leung VY. Concise review: The surface markers and identity of human mesenchymal stem cells. Stem Cells 2014; 32(6): 1408-19.
[41]
Chan CKF, Gulati GS, Sinha R, et al. Identification of the human skeletal stem cell Cell 2018; 175(1): 43-56 e21
[42]
Matic I, Matthews BG, Wang X, et al. Quiescent bone lining cells are a major source of osteoblasts during adulthood. Stem Cells 2016; 34(12): 2930-42.
[43]
Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012; 481(7382): 457-62.
[44]
Xie L, Zeng X, Hu J, Chen Q. Characterization of nestin, a selective marker for bone marrow derived mesenchymal stem cells. Stem Cells Int 2015; 2015: 762098.
[45]
Chen KG, Johnson KR, Robey PG. Mouse genetic analysis of bone marrow stem cell niches: Technological pitfalls, challenges, and translational considerations. Stem Cell Reports 2017; 9(5): 1343-58.
[46]
Kunisaki Y, Bruns I, Scheiermann C, et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 2013; 502(7473): 637-43.
[47]
Ramasamy SK, Kusumbe AP, Itkin T, Gur-Cohen S, Lapidot T, Adams RH. Regulation of hematopoiesis and osteogenesis by blood vessel-derived signals. Annu Rev Cell Dev Biol 2016; 32: 649-75.
[48]
Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 2014; 507(7492): 323-8.
[49]
Sacchetti B, Funari A, Michienzi S, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007; 131(2): 324-36.
[50]
Blocki A, Wang Y, Koch M, et al. Not all MSCs can act as pericytes: functional in vitro assays to distinguish pericytes from other mesenchymal stem cells in angiogenesis. Stem Cells Dev 2013; 22(17): 2347-55.
[51]
Herrmann M, Bara JJ, Sprecher CM, et al. Pericyte plasticity - comparative investigation of the angiogenic and multilineage potential of pericytes from different human tissues. Eur Cell Mater 2016; 31: 236-49.
[52]
Rasini V, Dominici M, Kluba T, et al. Mesenchymal stromal/stem cells markers in the human bone marrow. Cytotherapy 2013; 15(3): 292-306.
[53]
Lutolf MP, Gilbert PM, Blau HM. Designing materials to direct stem-cell fate. Nature 2009; 462(7272): 433-41.
[54]
Wu M, Chen G, Li YP. TGF-beta and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res 2016; 4: 16009.
[55]
Silva BC, Bilezikian JP. Parathyroid hormone: Anabolic and catabolic actions on the skeleton. Curr Opin Pharmacol 2015; 22: 41-50.
[56]
Baron R, Kneissel M. WNT signaling in bone homeostasis and disease: From human mutations to treatments. Nat Med 2013; 19(2): 179-92.
[57]
Florencio-Silva R, Sasso GR, Sasso-Cerri E, Simoes MJ, Cerri PS. Biology of bone tissue: Structure, function, and factors that influence bone cells. BioMed Res Int 2015; 2015: 421746.
[58]
Aicher A, Kollet O, Heeschen C, et al. The Wnt antagonist Dickkopf-1 mobilizes vasculogenic progenitor cells via activation of the bone marrow endosteal stem cell niche. Circ Res 2008; 103(8): 796-803.
[59]
Sugimoto A, Miyazaki A, Kawarabayashi K, et al. Piezo type mechanosensitive ion channel component 1 functions as a regulator of the cell fate determination of mesenchymal stem cells. Sci Rep 2017; 7(1): 17696.
[60]
Waghmare I, Page-McCaw A. Wnt Signaling in Stem Cell Maintenance and Differentiation in the Drosophila germarium. Genes 2018; 9(3)
[61]
Mottier-Pavie VI, Palacios V, Eliazer S, Scoggin S, Buszczak M. The Wnt pathway limits BMP signaling outside of the germline stem cell niche in Drosophila ovaries. Dev Biol 2016; 417(1): 50-62.
[62]
Fairfield H, Falank C, Harris E, et al. The skeletal cell-derived molecule sclerostin drives bone marrow adipogenesis. J Cell Physiol 2018; 233(2): 1156-67.
[63]
Cain CJ, Manilay JO. Hematopoietic stem cell fate decisions are regulated by Wnt antagonists: Comparisons and current controversies. Exp Hematol 2013; 41(1): 3-16.
[64]
Bao Q, Chen S, Qin H, et al. An appropriate Wnt/beta-catenin expression level during the remodeling phase is required for improved bone fracture healing in mice. Sci Rep 2017; 7(1): 2695.
[65]
Bao Q, Chen S, Qin H, et al. Constitutive beta-catenin activation in osteoblasts impairs terminal osteoblast differentiation and bone quality. Exp Cell Res 2017; 350(1): 123-31.
[66]
Kirstetter P, Anderson K, Porse BT, Jacobsen SE, Nerlov C. Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 2006; 7(10): 1048-56.
[67]
Kusumbe AP, Ramasamy SK, Itkin T, et al. Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature 2016; 532(7599): 380-4.
[68]
Liu Y, Berendsen AD, Jia S, et al. Intracellular VEGF regulates the balance between osteoblast and adipocyte differentiation. J Clin Invest 2012; 122(9): 3101-13.
[69]
Jung Y, Song J, Shiozawa Y, et al. Hematopoietic stem cells regulate mesenchymal stromal cell induction into osteoblasts thereby participating in the formation of the stem cell niche. Stem Cells 2008; 26(8): 2042-51.
[70]
Ejtehadifar M, Shamsasenjan K, Movassaghpour A, et al. The effect of hypoxia on mesenchymal stem cell biology. Adv Pharm Bull 2015; 5(2): 141-9.
[71]
Mao AS, Shin JW, Mooney DJ. Effects of substrate stiffness and cell-cell contact on mesenchymal stem cell differentiation. Biomaterials 2016; 98: 184-91.
[72]
Assis-Ribas T, Forni MF, Winnischofer SMB, Sogayar MC, Trombetta-Lima M. Extracellular matrix dynamics during mesenchymal stem cells differentiation. Dev Biol 2018; 437(2): 63-74.
[73]
Solimando AG, Brandl A, Mattenheimer K, et al. JAM-A as a prognostic factor and new therapeutic target in multiple myeloma. Leukemia 2018; 32(3): 736-43.
[74]
Arcangeli ML, Frontera V, Bardin F, et al. JAM-B regulates maintenance of hematopoietic stem cells in the bone marrow. Blood 2011; 118(17): 4609-19.
[75]
Lazarus HM, Haynesworth SE, Gerson SL, Caplan AI. Human bone marrow-derived Mesenchymal (stromal) Progenitor Cells (MPCs) cannot be recovered from peripheral blood progenitor cell collections. J Hematother 1997; 6(5): 447-55.
[76]
Richter R, Forssmann W, Henschler R. Current developments in mobilization of hematopoietic stem and progenitor cells and their interaction with niches in bone marrow. Transfus Med Hemother 2017; 44(3): 151-64.
[77]
McNulty MA, Virdi AS, Christopherson KW, Sena K, Frank RR, Sumner DR. Adult stem cell mobilization enhances intramembranous bone regeneration: A pilot study. Clinical orthopaedics and related research 2012; 470(9): 2503-12.
[78]
Kumar S, Ponnazhagan S. Mobilization of bone marrow mesenchymal stem cells in vivo augments bone healing in a mouse model of segmental bone defect. Bone 2012; 50(4): 1012-8.
[79]
Chen W, Li M, Cheng H, et al. Overexpression of the mesenchymal stem cell Cxcr4 gene in irradiated mice increases the homing capacity of these cells. Cell Biochem Biophys 2013; 67(3): 1181-91.
[80]
Wei JN, Cai F, Wang F, et al. Transplantation of CXCR4 overexpressed mesenchymal stem cells augments regeneration in degenerated intervertebral discs. DNA Cell Biol 2016; 35(5): 241-8.
[81]
Liu L, Yu Q, Lin J, et al. Hypoxia-inducible factor-1alpha is essential for hypoxia-induced mesenchymal stem cell mobilization into the peripheral blood. Stem Cells Dev 2011; 20(11): 1961-71.
[82]
Liu L, Yu Q, Fu S, et al. The CXCR4 antagonist AMD3100 promotes mesenchymal stem cell mobilization in rats preconditioned with the hypoxia-mimicking agent cobalt chloride. Stem Cells Dev 2018; 27(7): 466-78.
[83]
Ge T, Yu Q, Liu W, et al. Characterization of bone marrow-derived mesenchymal stem cells from dimethyloxallyl glycine-preconditioned mice: Evaluation of the feasibility of dimethyloxallyl glycine as a mobilization agent. Mol Med Rep 2016; 13(4): 3498-506.
[84]
Xu L, Li G. Circulating mesenchymal stem cells and their clinical implications. J Orthop Translat 2014; 2(1): 1-7.
[85]
Hoogduijn MJ, Verstegen MM, Engela AU, et al. No evidence for circulating mesenchymal stem cells in patients with organ injury. Stem Cells Dev 2014; 23(19): 2328-35.
[86]
Niemiro GM, Parel J, Beals J, et al. Kinetics of circulating progenitor cell mobilization during submaximal exercise. J Appl Physiol 2017; 122(3): 675-82.
[87]
Le Blanc K, Davies LC. MSCs-cells with many sides. Cytotherapy 2018; 20(3): 273-8.
[88]
Benisch P, Schilling T, Klein-Hitpass L, et al. The transcriptional profile of mesenchymal stem cell populations in primary osteoporosis is distinct and shows overexpression of osteogenic inhibitors. PLoS One 2012; 7(9): e45142.
[89]
Kohler J, Popov C, Klotz B, et al. Uncovering the cellular and molecular changes in tendon stem/progenitor cells attributed to tendon aging and degeneration. Aging Cell 2013; 12(6): 988-99.
[90]
Ganguly P, El-Jawhari JJ, Giannoudis PV, Burska AN, Ponchel F, Jones EA. Age-related changes in bone marrow mesenchymal stromal cells: A potential impact on osteoporosis and osteoarthritis development. Cell Transplant 2017; 26(9): 1520-9.
[91]
Ambrosi TH, Scialdone A, Graja A, et al. Adipocyte accumulation in the bone marrow during obesity and aging impairs stem cell-based hematopoietic and bone regenerationCell Stem Cell 2017; 20(6): 771-84 e6
[92]
Zimmermann EA, Schaible E, Bale H, et al. Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. Proc Natl Acad Sci USA 2011; 108(35): 14416-21.
[93]
Ritschka B, Storer M, Mas A, et al. The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration. Genes Dev 2017; 31(2): 172-83.
[94]
Neves J, Sousa-Victor P, Jasper H. Rejuvenating strategies for stem cell-based therapies in aging. Cell Stem Cell 2017; 20(2): 161-75.
[95]
Ebert R, Benisch P, Krug M, et al. Acute phase serum amyloid A induces proinflammatory cytokines and mineralization via toll-like receptor 4 in mesenchymal stem cells. Stem Cell Res 2015; 15(1): 231-9.
[96]
Serrano M. Senescence helps regeneration. Dev Cell 2014; 31(6): 671-2.
[97]
Jeon OH, Kim C, Laberge RM, et al. Local clearance of senescent cells attenuates the development of post-traumatic osteoarthritis and creates a pro-regenerative environment. Nat Med 2017; 23(6): 775-81.
[98]
Jakob F, Ebert R, Rudert M, et al. In situ guided tissue regeneration in musculoskeletal diseases and aging: Implementing pathology into tailored tissue engineering strategies. Cell Tissue Res 2012; 347(3): 725-35.
[99]
Holzapfel BM, Reichert JC, Schantz JT, et al. How smart do biomaterials need to be? A translational science and clinical point of view. Adv Drug Deliv Rev 2013; 65(4): 581-603.
[100]
Loebel C, Czekanska EM, Staudacher J, et al. The calcification potential of human MSCs can be enhanced by interleukin-1beta in osteogenic medium. J Tissue Eng Regen Med 2017; 11(2): 564-71.
[101]
Hofbauer LC, Rachner TD, Coleman RE, Jakob F. Endocrine aspects of bone metastases. Lancet Diabetes Endocrinol 2014; 2(6): 500-12.
[102]
Rucci N, Teti A. Osteomimicry: How the seed grows in the soil. Calcif Tissue Int 2018; 102(2): 131-40.
[103]
Plebanek MP, Angeloni NL, Vinokour E, et al. Pre-metastatic cancer exosomes induce immune surveillance by patrolling monocytes at the metastatic niche. Nat Commun 2017; 8(1): 1319.
[104]
Graham N, Qian BZ. Mesenchymal stromal cells: Emerging roles in bone metastasis. Int J Mol Sci 2018; 19(4)
[105]
Weilbaecher KN, Guise TA, McCauley LK. Cancer to bone: A fatal attraction. Nat Rev Cancer 2011; 11(6): 411-25.
[106]
Yu C, Shiozawa Y, Taichman RS, McCauley LK, Pienta K, Keller E. Prostate cancer and parasitism of the bone hematopoietic stem cell niche. Crit Rev Eukaryot Gene Expr 2012; 22(2): 131-48.
[107]
Lu H, Clauser KR, Tam WL, et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat Cell Biol 2014; 16(11): 1105-17.
[108]
Dhawan A, Friedrichs J, Bonin MV, et al. Breast cancer cells compete with hematopoietic stem and progenitor cells for intercellular adhesion molecule 1-mediated binding to the bone marrow microenvironment. Carcinogenesis 2016; 37(8): 759-67.
[109]
Wobus M, List C, Dittrich T, et al. Breast carcinoma cells modulate the chemoattractive activity of human bone marrow-derived mesenchymal stromal cells by interfering with CXCL12. Int J Cancer 2015; 136(1): 44-54.
[110]
Walker ND, Patel J, Munoz JL, et al. The bone marrow niche in support of breast cancer dormancy. Cancer Lett 2016; 380(1): 263-71.
[111]
Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425(6960): 841-6.
[112]
Diaz de la Guardia R, Lopez-Millan B, et al. Detailed characterization of mesenchymal stem/stromal cells from a large cohort of aml patients demonstrates a definitive link to treatment outcomes. Stem Cell Reports 2017; 8(6): 1573-86.
[113]
Doron B, Handu M, Kurre P. Concise review: Adaptation of the bone marrow stroma in hematopoietic malignancies: Current concepts and models. Stem Cells 2018; 36(3): 304-12.
[114]
Schinke C, Qu P, Mehdi SJ, et al. The pattern of Mesenchymal stem cell expression is an independent marker of outcome in multiple myeloma. Clin Cancer Res 2018; 24(12): 2913-9.
[115]
Xu S, De Veirman K, De Becker A, Vanderkerken K, Van Riet I. Mesenchymal stem cells in multiple myeloma: A therapeutical tool or target? Leukemia 2018; 32(7): 1500-14.
[116]
Coniglio SJ. Role of tumor-derived chemokines in osteolytic bone metastasis. Front Endocrinol 2018; 9: 313.
[117]
Steinbichler TB, Dudas J, Riechelmann H, Skvortsova II. The role of exosomes in cancer metastasis. Semin Cancer Biol 2017; 44: 170-81.
[118]
Liu Y, Cao X. Characteristics and significance of the pre-metastatic niche. Cancer Cell 2016; 30(5): 668-81.
[119]
Dotterweich J, Schlegelmilch K, Keller A, et al. Contact of myeloma cells induces a characteristic transcriptome signature in skeletal precursor cells implications for myeloma bone disease. Bone 2016; 93: 155-66.
[120]
Lapa C, Kircher S, Schirbel A, et al. Targeting CXCR4 with [(68)Ga]Pentixafor: A suitable theranostic approach in pleural mesothelioma? Oncotarget 2017; 8(57): 96732-7.
[121]
Herrmann K, Schottelius M, Lapa C, et al. First-in-human experience of cxcr4-directed endoradiotherapy with 177lu- and 90y-labeled pentixather in advanced-stage multiple myeloma with extensive intra- and extramedullary disease. J Nucl Med 2016; 57(2): 248-51.
[122]
Dotterweich J, Tower RJ, Brandl A, et al. The KISS1 receptor as an in vivo microenvironment imaging biomarker of multiple myeloma bone disease. PLoS One 2016; 11(5): e0155087.
[123]
Dotterweich J, Ebert R, Kraus S, Tower RJ, Jakob F, Schutze N. Mesenchymal stem cell contact promotes CCN1 splicing and transcription in myeloma cells. Cell Commun Signal 2014; 12: 36.
[124]
Peled A, Klein S, Beider K, Burger JA, Abraham M. Role of CXCL12 and CXCR4 in the pathogenesis of hematological malignancies. Cytokine 2018; 109: 11-6.
[125]
Socovich AM, Naba A. The cancer matrisome: From comprehensive characterization to biomarker discovery. Semin Cell Dev Biol 2018; pii: S1084-9521(17)30580-3.
[126]
Khan AB, Carpenter B, Santos ESP, et al. Redirection to the bone marrow improves T cell persistence and antitumor functions. J Clin Invest 2018; 128(5): 2010-24.
[127]
Gao X, Xu C, Asada N, Frenette PS. The hematopoietic stem cell niche: from embryo to adult. Development 2018; 145(2)
[128]
Zhao H, Achreja A, Iessi E, et al. The key role of extracellular vesicles in the metastatic process. Biochim Biophys Acta 2018; 1869(1): 64-77.
[129]
Hill BS, Pelagalli A, Passaro N, Zannetti A. Tumor-educated mesenchymal stem cells promote pro-metastatic phenotype. Oncotarget 2017; 8(42): 73296-311.
[130]
Batlle E, Clevers H. Cancer stem cells revisited. Nat Med 2017; 23(10): 1124-34.
[131]
Swami S, Johnson J, Bettinson LA, et al. Prevention of breast cancer skeletal metastases with parathyroid hormone. JCI Insight 2017; 2(17)
[132]
Wang X, Mooradian AD, Erdmann-Gilmore P, et al. Breast tumors educate the proteome of stromal tissue in an individualized but coordinated manner. Sci Signal 2017; 10(491): pii:eaam8065.
[133]
Chen XW, Yu TJ, Zhang J, et al. CYP4A in tumor-associated macrophages promotes pre-metastatic niche formation and metastasis. Oncogene 2017; 36(35): 5045-57.
[134]
Peinado H, Zhang H, Matei IR, et al. Pre-metastatic niches: Organ-specific homes for metastases. Nat Rev Cancer 2017; 17(5): 302-17.
[135]
Jablonska J, Lang S, Sionov RV, Granot Z. The regulation of pre-metastatic niche formation by neutrophils. Oncotarget 2017; 8(67): 112132-44.
[136]
Marturano-Kruik A, Nava MM, Yeager K, et al. Human bone perivascular niche-on-a-chip for studying metastatic colonization. Proc Natl Acad Sci USA 2018; 115(6): 1256-61.
[137]
Huber BC, Grabmaier U, Brunner S. Impact of parathyroid hormone on bone marrow-derived stem cell mobilization and migration. World J Stem Cells 2014; 6(5): 637-43.
[138]
Soki FN, Park SI, McCauley LK. The multifaceted actions of PTHrP in skeletal metastasis. Future Oncol 2012; 8(7): 803-17.
[139]
Rossnagl S, Ghura H, Groth C, et al. A subpopulation of stromal cells controls cancer cell homing to the bone marrow. Cancer Res 2018; 78(1): 129-42.
[140]
Shiozawa Y, Pedersen EA, Havens AM, et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin inv 2011; 121(4): 1298-312.
[141]
Bara JJ, Richards RG, Alini M, Stoddart MJ. Concise review: Bone marrow‐derived mesenchymal stem cells change phenotype following in vitro culture: Implications for basic research and the clinic. Stem Cells 2014; 32(7): 1713-23.
[142]
Bara JJ, Herrmann M, Evans CH, Miclau T, Ratcliffe A, Richards RG. Improving translation success of cell-based therapies in orthopaedics. J Orthop Res 2016; 34(1): 17-21.
[143]
Calvi LM, Link DC. The hematopoietic stem cell niche in homeostasis and disease. Blood 2015; 126(22): 2443-51.
[144]
He S, Sharpless NE. Senescence in Health and Disease. Cell 2017; 169(6): 1000-11.
[145]
Oh J, Lee YD, Wagers AJ. Stem cell aging: Mechanisms, regulators and therapeutic opportunities. Nat Med 2014; 20(8): 870-80.

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