Allergen Homologues, Pathogenesis-Related 1, Polygalacturonase, and Pectin Methyl Esterase from a Japanese Hop

Author(s): Seok Woo Jang, Kyoung Yong Jeong*, Ji Eun Yuk, Jongsun Lee, Kyung Hee Park, Jung-Won Park

Journal Name: Protein & Peptide Letters

Volume 28 , Issue 4 , 2021


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Background: Japanese hop is an important cause of weed pollinosis in East Asia. Its pollen is abundant in autumn. This pollen is known to be the cause of many allergic diseases. However, molecular characteristics of its allergens have not been elucidated.

Objective: In this study, we produced recombinant proteins of allergen homologues from Japanese hop by the analysis of expressed sequence tags (EST), and evaluated its allergenicity.

Methods: cDNA library was constructed using as little as 50 ng of total RNA from Japanese hop pollen. Allergen homologues were identified by the initial screening of 963 EST clones. Recombinant proteins were overexpressed in the E. coli expression system and purified using Ni-nitrilotriacetic acid-agarose. Purified proteins were analyzed by ELISA.

Results and Discussion: Japanese hop pathogenesis-related 1 protein (PR-1) shares 37.0 to 44.4% of amino acid sequence identity with Art v 2, Cuc m 3, and Cyn d 24. Pectin methyl esterase (PME) shows 23.2 to 50.2% of identities to Act d 7, Ole e 11, and Sal k 1. Polygalacturonase (PGs) shows 16.7 to 19.3% of identities to Phl p 13, Cry j 2, Cha o 2, Jun a 2, Pla a 2, and Pla or 2. IgE antibodies from Japanese hop allergy patients’ sera recognized PR-1 (3.4%), PME (13.8%), PGs (3.7%), and profilin (13.8%), respectively.

Conclusion: Novel allergenic components were identified, even though low IgE reactivity was displayed reflecting the low degree of cross-reactivity with other pollen allergens. We believe that these molecules have worth further studies.

Keywords: Pathogenesis-related 1, pectin methyl esterase, polygalacturonase, pollinosis, allergic diseases, Japanese hop.

[1]
Radauer, C.; Bublin, M.; Wagner, S.; Mari, A.; Breiteneder, H. Allergens are distributed into few protein families and possess a restricted number of biochemical functions. J. Allergy Clin. Immunol., 2008, 121(4), 847-52.e7.
[http://dx.doi.org/10.1016/j.jaci.2008.01.025] [PMID: 18395549]
[2]
Mari, A.; Rasi, C.; Palazzo, P.; Scala, E. Allergen databases: current status and perspectives. Curr. Allergy Asthma Rep., 2009, 9(5), 376-383.
[http://dx.doi.org/10.1007/s11882-009-0055-9] [PMID: 19671381]
[3]
Dall’antonia, F.; Pavkov-Keller, T.; Zangger, K.; Keller, W. Structure of allergens and structure based epitope predictions. Methods, 2014, 66(1), 3-21.
[http://dx.doi.org/10.1016/j.ymeth.2013.07.024] [PMID: 23891546]
[4]
Park, H.J.; Lee, J.H.; Park, K.H.; Kim, K.R.; Han, M.J.; Choe, H.; Oh, J.W.; Hong, C.S. A six-year study on the changes in airborne pollen counts and skin positivity rates in Korea: 2008-2013. Yonsei Med. J., 2016, 57(3), 714-720.
[http://dx.doi.org/10.3349/ymj.2016.57.3.714] [PMID: 26996572]
[5]
Sung, M.; Kim, S.W.; Kim, J.H.; Lim, D.H. Regional difference of causative pollen in children with allergic rhinitis. J. Korean Med. Sci., 2017, 32(6), 926-932.
[http://dx.doi.org/10.3346/jkms.2017.32.6.926] [PMID: 28480649]
[6]
Kim, K.R.; Kim, M.; Choe, H.S.; Han, M.J.; Lee, H.R.; Oh, J.W.; Kim, B.J. A biology-driven receptor model for daily pollen allergy risk in Korea based on Weibull probability density function. Int. J. Biometeorol., 2017, 61(2), 259-272.
[http://dx.doi.org/10.1007/s00484-016-1208-x] [PMID: 27387542]
[7]
Park, H.S.; Nahm, D.H.; Suh, C.H.; Lee, S.M.; Choi, S.Y.; Jung, K.S.; Lee, S.Y.; Park, K. Evidence of Hop Japanese pollinosis in Korea: IgE sensitization and identification of allergenic components. J. Allergy Clin. Immunol., 1997, 100(4), 475-479.
[http://dx.doi.org/10.1016/S0091-6749(97)70138-6] [PMID: 9338540]
[8]
Kim, K.H.; Kim, K.T.; Lee, S.K.; Park, H.S.; Lee, Y.M. Sensitization rates for inhalant allergens in patients with respiratory allergy in Busan. Korean J. Asthma Allergy Clin. Innumol., 2005, 25(1), 59-63.
[9]
Hong, C.S.; Hwang, Y.; Oh, S.H.; Kim, H.J.; Huh, K.B.; Lee, S.Y. Survey of the airborne pollens in Seoul, Korea. Yonsei Med. J., 1986, 27(2), 114-120.
[http://dx.doi.org/10.3349/ymj.1986.27.2.114] [PMID: 3751125]
[10]
Lewis, W.H.; Vinay, P.; Zenger, V.E. Airborne and allergic pollen of North America; The Johns Hopkins University Press: Baltimore, London, 1983.
[11]
Esch, R.E.; Bush, R.K. Aerobiology of outdoor allergens. In: Middleton’s allergy princiles and practice. Adkinson, N.F.Jr.; Yunginger, J.W.; Busse, W.W.; Bochner, B.S.; Holgate, S.T.; Simons, F.E.R.; Eds., 6th ed; Mosby: St. Louis, 2003, pp. 529-555.
[12]
Potter, P.C.; Cadman, A. Pollen allergy in South Africa. Clin. Exp. Allergy, 1996, 26(12), 1347-1354.
[http://dx.doi.org/10.1111/j.1365-2222.1996.tb00535.x] [PMID: 9027434]
[13]
Solomon, W.R.; Weber, R.W.; Dolen, W.K. Common allergenic pollen and fungi. In: Allergy, asthma and immunology from infancy to adulthood. Bierman, C.W.; Pearlman, D.S.; Shapiro, G.G.; Busse, W.W.; Eds., 3rd ed; WB Saunders: Philadelphia, 1996, pp. 93-114.
[14]
Ye, Y.M.; Lee, S.K.; Kim, S.H.; Nahm, D.H.; Suh, C.H.; Park, H.S. Changes of serum cytokines after the long term immunotherapy with Japanese hop pollen extracts. J. Korean Med. Sci., 2006, 21(5), 805-810.
[http://dx.doi.org/10.3346/jkms.2006.21.5.805] [PMID: 17043410]
[15]
Lee, G.W.; Choi, G.S.; Kim, J.E.; Jin, H.J.; Kim, J.H. Changes in sensitization rates to pollen allergens in allergic patients in the southern part of Gyeonggi province over the last 10 years. Korean. J. Asthma Allergy Clin. Immunol, 2011, 31(1), 33-40.
[16]
Nam, D.K.; Park, H.S.; Oh, S.H.; Hong, C.S. Skin reactivity and the detection of specific IgE to the pollen of Humulus japonicus. Korean J. Med., 1988, 35(2), 213-228.
[17]
Park, H.S.; Jung, K.S.; Jee, S.Y.; Hong, S.H.; Kim, H.Y.; Nahm, D.H. Are there any links between Hop Japanese pollen and other weed pollens or food allergens on skin prick tests? Allergy Asthma Proc., 2001, 22(1), 43-46.
[http://dx.doi.org/10.2500/108854101778249186] [PMID: 11227917]
[18]
Shida, T.; Akiyama, K.; Hasegawa, M.; Maeda, Y.; Taniguchi, M.; Mori, A.; Tomita, S.; Yamamoto, N.; Ishii, T.; Saito, A.; Yasueda, H. Change in skin reactivity to common allergens in allergic patients over a 30-year period. Association with aeroallergen load. Arerugi, 2000, 49(11), 1074-1086.
[PMID: 11193459]
[19]
Park, J.W.; Ko, S.H.; Kim, C.W.; Jeoung, B.J.; Hong, C.S. Identification and characterization of the major allergen of the Humulus japonicus pollen. Clin. Exp. Allergy, 1999, 29(8), 1080-1086.
[http://dx.doi.org/10.1046/j.1365-2222.1999.00615.x] [PMID: 10457112]
[20]
Asensio, T.; Crespo, J.F.; Sanchez-Monge, R.; Lopez-Torrejon, G.; Somoza, M.L.; Rodriguez, J.; Salcedo, G. Novel plant pathogenesis-related protein family involved in food allergy. J. Allergy Clin. Immunol., 2004, 114(4), 896-899.
[http://dx.doi.org/10.1016/j.jaci.2004.06.014] [PMID: 15480331]
[21]
Chow, L.P.; Chiu, L.L.; Khoo, K.H.; Peng, H.J.; Yang, S.Y.; Huang, S.W.; Su, S.N. Purification and structural analysis of the novel glycoprotein allergen Cyn d 24, a pathogenesis-related protein PR-1, from Bermuda grass pollen. FEBS J., 2005, 272(24), 6218-6227.
[http://dx.doi.org/10.1111/j.1742-4658.2005.05000.x] [PMID: 16336260]
[22]
Suck, R.; Petersen, A.; Hagen, S.; Cromwell, O.; Becker, W.M.; Fiebig, H. Complementary DNA cloning and expression of a newly recognized high molecular mass allergen phl p 13 from timothy grass pollen (Phleum pratense). Clin. Exp. Allergy, 2000, 30(3), 324-332.
[http://dx.doi.org/10.1046/j.1365-2222.2000.00843.x] [PMID: 10691889]
[23]
Wang, D.W.; Ni, W.W.; Zhou, Y.J.; Huang, W.; Cao, M.D.; Meng, L.; Wei, J.F. Expression, purification and epitope analysis of Pla a 2 allergen from Platanus acerifolia pollen. Mol. Med. Rep., 2018, 17(1), 394-399.
[PMID: 29115430]
[24]
Ibarrola, I.; Arilla, M.C.; Martínez, A.; Asturias, J.A. Identification of a polygalacturonase as a major allergen (Pla a 2) from Platanus acerifolia pollen. J. Allergy Clin. Immunol., 2004, 113(6), 1185-1191.
[http://dx.doi.org/10.1016/j.jaci.2004.02.031] [PMID: 15208603]
[25]
Jeong, K.Y.; Han, I.S.; Choi, S.Y.; Lee, J.H.; Lee, J.S.; Hong, C.S.; Park, J.W. Allergenicity of recombinant profilins from Japanese hop, Humulus japonicus. J. Investig. Allergol. Clin. Immunol., 2013, 23(5), 345-350.
[PMID: 24260980]
[26]
van Ree, R. Analytic aspects of the standardization of allergenic extracts. Allergy, 1997, 52(8), 795-805.
[http://dx.doi.org/10.1111/j.1398-9995.1997.tb02150.x] [PMID: 9284978]
[27]
Durham, S.R.; Walker, S.M.; Varga, E.M.; Jacobson, M.R.; O’Brien, F.; Noble, W.; Till, S.J.; Hamid, Q.A.; Nouri-Aria, K.T. Long-term clinical efficacy of grass-pollen immunotherapy. N. Engl. J. Med., 1999, 341(7), 468-475.
[http://dx.doi.org/10.1056/NEJM199908123410702] [PMID: 10441602]
[28]
van Hage-Hamsten, M.; Johansson, E.; Roquet, A.; Peterson, C.; Andersson, M.; Greiff, L.; Vrtala, S.; Valenta, R.; Grönneberg, R. Nasal challenges with recombinant derivatives of the major birch pollen allergen Bet v 1 induce fewer symptoms and lower mediator release than rBet v 1 wild-type in patients with allergic rhinitis. Clin. Exp. Allergy, 2002, 32(10), 1448-1453.
[http://dx.doi.org/10.1046/j.1365-2745.2002.01495.x] [PMID: 12372124]
[29]
Park, H.S.; Nahm, D.H.; Kim, H.Y.; Suh, Y.J.; Cho, J.W.; Kim, S.S.; Lee, S.K.; Jung, K.S. Clinical and immunologic changes after allergen immunotherapy with Hop Japanese pollen. Ann. Allergy Asthma Immunol., 2001, 86(4), 444-448.
[http://dx.doi.org/10.1016/S1081-1206(10)62493-3] [PMID: 11345290]
[30]
Valenta, R.; Kraft, D. Recombinant allergen molecules: tools to study effector cell activation. Immunol. Rev., 2001, 179(1), 119-127.
[http://dx.doi.org/10.1034/j.1600-065X.2001.790112.x] [PMID: 11292015]
[31]
Dhondalay, G.K.; Rael, E.; Acharya, S.; Zhang, W.; Sampath, V.; Galli, S.J.; Tibshirani, R.; Boyd, S.D.; Maecker, H.; Nadeau, K.C.; Andorf, S. Food allergy and omics. J. Allergy Clin. Immunol., 2018, 141(1), 20-29.
[http://dx.doi.org/10.1016/j.jaci.2017.11.007] [PMID: 29307411]
[32]
Jeong, K.Y.; Tungtrongchitr, A. Allergens at Asian Homes. Curr. Protein Pept. Sci., 2020, 21(2), 112-113.
[http://dx.doi.org/10.2174/138920372102200129143611] [PMID: 32167036]
[33]
Jeong, K.Y.; Lee, J.; Mistrello, G.; Park, K.H.; Park, J.W. IgE cross-reactivity between Humulus japonicus and Humulus lupulus. Yonsei Med. J., 2018, 59(7), 852-856.
[http://dx.doi.org/10.3349/ymj.2018.59.7.852] [PMID: 30091318]
[34]
Pomés, A. Relevant B cell epitopes in allergic disease. Int. Arch. Allergy Immunol., 2010, 152(1), 1-11.
[http://dx.doi.org/10.1159/000260078] [PMID: 19940500]
[35]
Arilla, M.C.; Ibarrola, I.; Puente, Y.; Daza, J.C.; Martínez, A.; Asturias, J.A. Cloning, expression and characterization of mugwort pollen allergen Art v 2, a pathogenesis-related protein from family group 1. Mol. Immunol., 2007, 44(15), 3653-3660.
[http://dx.doi.org/10.1016/j.molimm.2007.04.022] [PMID: 17521730]
[36]
Carnés, J.; Fernández-Caldas, E.; Marina, A.; Alonso, C.; Lahoz, C.; Colás, C.; Lezaun, A. Immunochemical characterization of Russian thistle (Salsola kali) pollen extracts. Purification of the allergen Sal k 1. Allergy, 2003, 58(11), 1152-1156.
[http://dx.doi.org/10.1034/j.1398-9995.2003.00269.x] [PMID: 14616126]
[37]
Barderas, R.; García-Sellés, J.; Salamanca, G.; Colás, C.; Barber, D.; Rodríguez, R.; Villalba, M. A pectin methylesterase as an allergenic marker for the sensitization to Russian thistle (Salsola kali) pollen. Clin. Exp. Allergy, 2007, 37(7), 1111-1119.
[http://dx.doi.org/10.1111/j.1365-2222.2007.02744.x] [PMID: 17581207]
[38]
Assarehzadegan, M.A.; Sankian, M.; Jabbari, F.; Tehrani, M.; Varasteh, A. Expression of the recombinant major allergen of Salsola kali pollen (Sal k 1) and comparison with its low-immunoglobulin E-binding mutant. Allergol. Int., 2010, 59(2), 213-222.
[http://dx.doi.org/10.2332/allergolint.09-OA-0155] [PMID: 20414052]
[39]
Ohtsuki, T.; Taniguchi, Y.; Kohno, K.; Fukuda, S.; Usui, M.; Kurimoto, M. Cry j 2, a major allergen of Japanese cedar pollen, shows polymethylgalacturonase activity. Allergy, 1995, 50(6), 483-488.
[http://dx.doi.org/10.1111/j.1398-9995.1995.tb01183.x] [PMID: 7573841]
[40]
Park, K.H.; Lee, J.; Lee, J.Y.; Lee, S.C.; Sim, D.W.; Shin, J.U.; Park, C.O.; Lee, J.H.; Lee, K.H.; Jeong, K.Y.; Park, J.W. Sensitization to various minor house dust mite allergens is greater in patients with atopic dermatitis than in those with respiratory allergic disease. Clin. Exp. Allergy, 2018, 48(8), 1050-1058.
[http://dx.doi.org/10.1111/cea.13164] [PMID: 29700921]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 28
ISSUE: 4
Year: 2021
Published on: 19 May, 2021
Page: [362 - 371]
Pages: 10
DOI: 10.2174/0929866527666200813201924
Price: $65

Article Metrics

PDF: 41