Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans

Kui Liu, Quan Zhen Li, Angelica M. Delgado-Vega, Anna Karin Abelson, Elena Sánchez, Jennifer A. Kelly, Li Li, Yang Liu, Jinchun Zhou, Mei Yan, Qiu Ye, Shenxi Liu, Chun Xie, Xin J. Zhou, Sharon A. Chung, Bernardo Pons-Estel, Torsten Witte, Enrique De Ramón, Sang Cheol Bae, Nadia BarizzoneGian Domenico Sebastiani, Joan T. Merrill, Peter K. Gregersen, Gary G. Gilkeson, Robert P. Kimberly, Timothy J. Vyse, Il Kim, Sandra D'Alfonso, Javier Martin, John B. Harley, Lindsey A. Criswell, Edward K. Wakeland, Marta E. Alarcón-Riquelme, Chandra Mohan, Maria Giovanna Danieli, Mauro Galeazzi, Patrizia Rovere Querini, Sergio Migliaresi, Hugo R. Scherbarth, Jorge A. Lopez, Estela L. Motta, Susana Gamron, Cristina Drenkard, Emilia Menso, Alberto Allievi, Guillermo A. Tate, José L. Presas, Simon A. Palatnik, Marcelo Abdala, Mariela Bearzotti, Alejandro Alvarellos, Francisco Caeiro, Ana Bertoli, Sergio Paira, Susana Roverano, Cesar E. Graf, Estela Bertero, Cesar Caprarulo, Griselda Buchanan, Carolina Guillerón, Sebastian Grimaudo, Jorge Manni, Luis J. Catoggio, Enrique R. Soriano, Carlos D. Santos, Cristina Prigione, Fernando A. Ramos, Sandra M. Navarro, Guillermo A. Berbotto, Marisa Jorfen, Elisa J. Romero, Mercedes A. Garcia, Juan C. Marcos, Ana I. Marcos, Carlos E. Perandones, Alicia Eimon, Cristina G. Battagliotti, K. Armadi-Simab, Wolfgang L. Gross, Erika Gromnica-Ihle, Hans Hartmut Peter, Karin Manger, Sebastian Schnarr, Henning Zeidler, Reinhold E. Schmidt, Norberto Ortego, José L. Callejas, Juan Jiménez-Alonso, Mario Sabio, Julio Sánchez-Román, Francisco J. Garcia-Hernandez, Mayte Camps, Miguel Angel López-Nevot, Maria F. González-Escribano, Carl Langefeld, Betty Tsao, Chaim Jacob

Research output: Contribution to journalArticle

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Abstract

Immune-mediated nephritis contributes to disease in systemic lupus erythematosus, Goodpasture syndrome (caused by antibodies specific for glomerular basement membrane [anti-GBM antibodies]), and spontaneous lupus nephritis. Inbred mouse strains differ in susceptibility to anti-GBM antibody-induced and spontaneous lupus nephritis. This study sought to clarify the genetic and molecular factors that may be responsible for enhanced immune-mediated renal disease in these models. When the kidneys of 3 mouse strains sensitive to anti-GBM antibody-induced nephritis were compared with those of 2 control strains using microarray analysis, one-fifth of the underexpressed genes belonged to the kallikrein gene family, which encodes serine esterases. Mouse strains that upregulated renal and urinary kallikreins exhibited less evidence of disease. Antagonizing the kallikrein pathway augmented disease, while agonists dampened the severity of anti-GBM antibody-induced nephritis. In addition, nephritis-sensitive mouse strains had kallikrein haplotypes that were distinct from those of control strains, including several regulatory polymorphisms, some of which were associated with functional consequences. Indeed, increased susceptibility to anti-GBM antibody-induced nephritis and spontaneous lupus nephritis was achieved by breeding mice with a genetic interval harboring the kallikrein genes onto a disease-resistant background. Finally, both human SLE and spontaneous lupus nephritis were found to be associated with kallikrein genes, particularly KLK1 and the KLK3 promoter, when DNA SNPs from independent cohorts of SLE patients and controls were compared. Collectively, these studies suggest that kallikreins are protective disease-associated genes in anti-GBM antibody-induced nephritis and lupus.

Original languageEnglish (US)
Pages (from-to)911-923
Number of pages13
JournalJournal of Clinical Investigation
Volume119
Issue number4
DOIs
StatePublished - Apr 1 2009

Fingerprint

Glomerular Basement Membrane
Kallikreins
Nephritis
Lupus Nephritis
Anti-Idiotypic Antibodies
Antibodies
Genes
Kidney
Anti-Glomerular Basement Membrane Disease
Tissue Kallikreins
Inbred Strains Mice
Microarray Analysis
Systemic Lupus Erythematosus
Haplotypes
Breeding
Single Nucleotide Polymorphism
antiglomerular basement membrane antibody
Molecular Biology
DNA

ASJC Scopus subject areas

  • Medicine(all)

Cite this

Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans. / Liu, Kui; Li, Quan Zhen; Delgado-Vega, Angelica M.; Abelson, Anna Karin; Sánchez, Elena; Kelly, Jennifer A.; Li, Li; Liu, Yang; Zhou, Jinchun; Yan, Mei; Ye, Qiu; Liu, Shenxi; Xie, Chun; Zhou, Xin J.; Chung, Sharon A.; Pons-Estel, Bernardo; Witte, Torsten; De Ramón, Enrique; Bae, Sang Cheol; Barizzone, Nadia; Sebastiani, Gian Domenico; Merrill, Joan T.; Gregersen, Peter K.; Gilkeson, Gary G.; Kimberly, Robert P.; Vyse, Timothy J.; Kim, Il; D'Alfonso, Sandra; Martin, Javier; Harley, John B.; Criswell, Lindsey A.; Wakeland, Edward K.; Alarcón-Riquelme, Marta E.; Mohan, Chandra; Danieli, Maria Giovanna; Galeazzi, Mauro; Querini, Patrizia Rovere; Migliaresi, Sergio; Scherbarth, Hugo R.; Lopez, Jorge A.; Motta, Estela L.; Gamron, Susana; Drenkard, Cristina; Menso, Emilia; Allievi, Alberto; Tate, Guillermo A.; Presas, José L.; Palatnik, Simon A.; Abdala, Marcelo; Bearzotti, Mariela; Alvarellos, Alejandro; Caeiro, Francisco; Bertoli, Ana; Paira, Sergio; Roverano, Susana; Graf, Cesar E.; Bertero, Estela; Caprarulo, Cesar; Buchanan, Griselda; Guillerón, Carolina; Grimaudo, Sebastian; Manni, Jorge; Catoggio, Luis J.; Soriano, Enrique R.; Santos, Carlos D.; Prigione, Cristina; Ramos, Fernando A.; Navarro, Sandra M.; Berbotto, Guillermo A.; Jorfen, Marisa; Romero, Elisa J.; Garcia, Mercedes A.; Marcos, Juan C.; Marcos, Ana I.; Perandones, Carlos E.; Eimon, Alicia; Battagliotti, Cristina G.; Armadi-Simab, K.; Gross, Wolfgang L.; Gromnica-Ihle, Erika; Peter, Hans Hartmut; Manger, Karin; Schnarr, Sebastian; Zeidler, Henning; Schmidt, Reinhold E.; Ortego, Norberto; Callejas, José L.; Jiménez-Alonso, Juan; Sabio, Mario; Sánchez-Román, Julio; Garcia-Hernandez, Francisco J.; Camps, Mayte; López-Nevot, Miguel Angel; González-Escribano, Maria F.; Langefeld, Carl; Tsao, Betty; Jacob, Chaim.

In: Journal of Clinical Investigation, Vol. 119, No. 4, 01.04.2009, p. 911-923.

Research output: Contribution to journalArticle

Liu, K, Li, QZ, Delgado-Vega, AM, Abelson, AK, Sánchez, E, Kelly, JA, Li, L, Liu, Y, Zhou, J, Yan, M, Ye, Q, Liu, S, Xie, C, Zhou, XJ, Chung, SA, Pons-Estel, B, Witte, T, De Ramón, E, Bae, SC, Barizzone, N, Sebastiani, GD, Merrill, JT, Gregersen, PK, Gilkeson, GG, Kimberly, RP, Vyse, TJ, Kim, I, D'Alfonso, S, Martin, J, Harley, JB, Criswell, LA, Wakeland, EK, Alarcón-Riquelme, ME, Mohan, C, Danieli, MG, Galeazzi, M, Querini, PR, Migliaresi, S, Scherbarth, HR, Lopez, JA, Motta, EL, Gamron, S, Drenkard, C, Menso, E, Allievi, A, Tate, GA, Presas, JL, Palatnik, SA, Abdala, M, Bearzotti, M, Alvarellos, A, Caeiro, F, Bertoli, A, Paira, S, Roverano, S, Graf, CE, Bertero, E, Caprarulo, C, Buchanan, G, Guillerón, C, Grimaudo, S, Manni, J, Catoggio, LJ, Soriano, ER, Santos, CD, Prigione, C, Ramos, FA, Navarro, SM, Berbotto, GA, Jorfen, M, Romero, EJ, Garcia, MA, Marcos, JC, Marcos, AI, Perandones, CE, Eimon, A, Battagliotti, CG, Armadi-Simab, K, Gross, WL, Gromnica-Ihle, E, Peter, HH, Manger, K, Schnarr, S, Zeidler, H, Schmidt, RE, Ortego, N, Callejas, JL, Jiménez-Alonso, J, Sabio, M, Sánchez-Román, J, Garcia-Hernandez, FJ, Camps, M, López-Nevot, MA, González-Escribano, MF, Langefeld, C, Tsao, B & Jacob, C 2009, 'Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans', Journal of Clinical Investigation, vol. 119, no. 4, pp. 911-923. https://doi.org/10.1172/JCI36728
Liu, Kui ; Li, Quan Zhen ; Delgado-Vega, Angelica M. ; Abelson, Anna Karin ; Sánchez, Elena ; Kelly, Jennifer A. ; Li, Li ; Liu, Yang ; Zhou, Jinchun ; Yan, Mei ; Ye, Qiu ; Liu, Shenxi ; Xie, Chun ; Zhou, Xin J. ; Chung, Sharon A. ; Pons-Estel, Bernardo ; Witte, Torsten ; De Ramón, Enrique ; Bae, Sang Cheol ; Barizzone, Nadia ; Sebastiani, Gian Domenico ; Merrill, Joan T. ; Gregersen, Peter K. ; Gilkeson, Gary G. ; Kimberly, Robert P. ; Vyse, Timothy J. ; Kim, Il ; D'Alfonso, Sandra ; Martin, Javier ; Harley, John B. ; Criswell, Lindsey A. ; Wakeland, Edward K. ; Alarcón-Riquelme, Marta E. ; Mohan, Chandra ; Danieli, Maria Giovanna ; Galeazzi, Mauro ; Querini, Patrizia Rovere ; Migliaresi, Sergio ; Scherbarth, Hugo R. ; Lopez, Jorge A. ; Motta, Estela L. ; Gamron, Susana ; Drenkard, Cristina ; Menso, Emilia ; Allievi, Alberto ; Tate, Guillermo A. ; Presas, José L. ; Palatnik, Simon A. ; Abdala, Marcelo ; Bearzotti, Mariela ; Alvarellos, Alejandro ; Caeiro, Francisco ; Bertoli, Ana ; Paira, Sergio ; Roverano, Susana ; Graf, Cesar E. ; Bertero, Estela ; Caprarulo, Cesar ; Buchanan, Griselda ; Guillerón, Carolina ; Grimaudo, Sebastian ; Manni, Jorge ; Catoggio, Luis J. ; Soriano, Enrique R. ; Santos, Carlos D. ; Prigione, Cristina ; Ramos, Fernando A. ; Navarro, Sandra M. ; Berbotto, Guillermo A. ; Jorfen, Marisa ; Romero, Elisa J. ; Garcia, Mercedes A. ; Marcos, Juan C. ; Marcos, Ana I. ; Perandones, Carlos E. ; Eimon, Alicia ; Battagliotti, Cristina G. ; Armadi-Simab, K. ; Gross, Wolfgang L. ; Gromnica-Ihle, Erika ; Peter, Hans Hartmut ; Manger, Karin ; Schnarr, Sebastian ; Zeidler, Henning ; Schmidt, Reinhold E. ; Ortego, Norberto ; Callejas, José L. ; Jiménez-Alonso, Juan ; Sabio, Mario ; Sánchez-Román, Julio ; Garcia-Hernandez, Francisco J. ; Camps, Mayte ; López-Nevot, Miguel Angel ; González-Escribano, Maria F. ; Langefeld, Carl ; Tsao, Betty ; Jacob, Chaim. / Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans. In: Journal of Clinical Investigation. 2009 ; Vol. 119, No. 4. pp. 911-923.
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title = "Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans",
abstract = "Immune-mediated nephritis contributes to disease in systemic lupus erythematosus, Goodpasture syndrome (caused by antibodies specific for glomerular basement membrane [anti-GBM antibodies]), and spontaneous lupus nephritis. Inbred mouse strains differ in susceptibility to anti-GBM antibody-induced and spontaneous lupus nephritis. This study sought to clarify the genetic and molecular factors that may be responsible for enhanced immune-mediated renal disease in these models. When the kidneys of 3 mouse strains sensitive to anti-GBM antibody-induced nephritis were compared with those of 2 control strains using microarray analysis, one-fifth of the underexpressed genes belonged to the kallikrein gene family, which encodes serine esterases. Mouse strains that upregulated renal and urinary kallikreins exhibited less evidence of disease. Antagonizing the kallikrein pathway augmented disease, while agonists dampened the severity of anti-GBM antibody-induced nephritis. In addition, nephritis-sensitive mouse strains had kallikrein haplotypes that were distinct from those of control strains, including several regulatory polymorphisms, some of which were associated with functional consequences. Indeed, increased susceptibility to anti-GBM antibody-induced nephritis and spontaneous lupus nephritis was achieved by breeding mice with a genetic interval harboring the kallikrein genes onto a disease-resistant background. Finally, both human SLE and spontaneous lupus nephritis were found to be associated with kallikrein genes, particularly KLK1 and the KLK3 promoter, when DNA SNPs from independent cohorts of SLE patients and controls were compared. Collectively, these studies suggest that kallikreins are protective disease-associated genes in anti-GBM antibody-induced nephritis and lupus.",
author = "Kui Liu and Li, {Quan Zhen} and Delgado-Vega, {Angelica M.} and Abelson, {Anna Karin} and Elena S{\'a}nchez and Kelly, {Jennifer A.} and Li Li and Yang Liu and Jinchun Zhou and Mei Yan and Qiu Ye and Shenxi Liu and Chun Xie and Zhou, {Xin J.} and Chung, {Sharon A.} and Bernardo Pons-Estel and Torsten Witte and {De Ram{\'o}n}, Enrique and Bae, {Sang Cheol} and Nadia Barizzone and Sebastiani, {Gian Domenico} and Merrill, {Joan T.} and Gregersen, {Peter K.} and Gilkeson, {Gary G.} and Kimberly, {Robert P.} and Vyse, {Timothy J.} and Il Kim and Sandra D'Alfonso and Javier Martin and Harley, {John B.} and Criswell, {Lindsey A.} and Wakeland, {Edward K.} and Alarc{\'o}n-Riquelme, {Marta E.} and Chandra Mohan and Danieli, {Maria Giovanna} and Mauro Galeazzi and Querini, {Patrizia Rovere} and Sergio Migliaresi and Scherbarth, {Hugo R.} and Lopez, {Jorge A.} and Motta, {Estela L.} and Susana Gamron and Cristina Drenkard and Emilia Menso and Alberto Allievi and Tate, {Guillermo A.} and Presas, {Jos{\'e} L.} and Palatnik, {Simon A.} and Marcelo Abdala and Mariela Bearzotti and Alejandro Alvarellos and Francisco Caeiro and Ana Bertoli and Sergio Paira and Susana Roverano and Graf, {Cesar E.} and Estela Bertero and Cesar Caprarulo and Griselda Buchanan and Carolina Guiller{\'o}n and Sebastian Grimaudo and Jorge Manni and Catoggio, {Luis J.} and Soriano, {Enrique R.} and Santos, {Carlos D.} and Cristina Prigione and Ramos, {Fernando A.} and Navarro, {Sandra M.} and Berbotto, {Guillermo A.} and Marisa Jorfen and Romero, {Elisa J.} and Garcia, {Mercedes A.} and Marcos, {Juan C.} and Marcos, {Ana I.} and Perandones, {Carlos E.} and Alicia Eimon and Battagliotti, {Cristina G.} and K. Armadi-Simab and Gross, {Wolfgang L.} and Erika Gromnica-Ihle and Peter, {Hans Hartmut} and Karin Manger and Sebastian Schnarr and Henning Zeidler and Schmidt, {Reinhold E.} and Norberto Ortego and Callejas, {Jos{\'e} L.} and Juan Jim{\'e}nez-Alonso and Mario Sabio and Julio S{\'a}nchez-Rom{\'a}n and Garcia-Hernandez, {Francisco J.} and Mayte Camps and L{\'o}pez-Nevot, {Miguel Angel} and Gonz{\'a}lez-Escribano, {Maria F.} and Carl Langefeld and Betty Tsao and Chaim Jacob",
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TY - JOUR

T1 - Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans

AU - Liu, Kui

AU - Li, Quan Zhen

AU - Delgado-Vega, Angelica M.

AU - Abelson, Anna Karin

AU - Sánchez, Elena

AU - Kelly, Jennifer A.

AU - Li, Li

AU - Liu, Yang

AU - Zhou, Jinchun

AU - Yan, Mei

AU - Ye, Qiu

AU - Liu, Shenxi

AU - Xie, Chun

AU - Zhou, Xin J.

AU - Chung, Sharon A.

AU - Pons-Estel, Bernardo

AU - Witte, Torsten

AU - De Ramón, Enrique

AU - Bae, Sang Cheol

AU - Barizzone, Nadia

AU - Sebastiani, Gian Domenico

AU - Merrill, Joan T.

AU - Gregersen, Peter K.

AU - Gilkeson, Gary G.

AU - Kimberly, Robert P.

AU - Vyse, Timothy J.

AU - Kim, Il

AU - D'Alfonso, Sandra

AU - Martin, Javier

AU - Harley, John B.

AU - Criswell, Lindsey A.

AU - Wakeland, Edward K.

AU - Alarcón-Riquelme, Marta E.

AU - Mohan, Chandra

AU - Danieli, Maria Giovanna

AU - Galeazzi, Mauro

AU - Querini, Patrizia Rovere

AU - Migliaresi, Sergio

AU - Scherbarth, Hugo R.

AU - Lopez, Jorge A.

AU - Motta, Estela L.

AU - Gamron, Susana

AU - Drenkard, Cristina

AU - Menso, Emilia

AU - Allievi, Alberto

AU - Tate, Guillermo A.

AU - Presas, José L.

AU - Palatnik, Simon A.

AU - Abdala, Marcelo

AU - Bearzotti, Mariela

AU - Alvarellos, Alejandro

AU - Caeiro, Francisco

AU - Bertoli, Ana

AU - Paira, Sergio

AU - Roverano, Susana

AU - Graf, Cesar E.

AU - Bertero, Estela

AU - Caprarulo, Cesar

AU - Buchanan, Griselda

AU - Guillerón, Carolina

AU - Grimaudo, Sebastian

AU - Manni, Jorge

AU - Catoggio, Luis J.

AU - Soriano, Enrique R.

AU - Santos, Carlos D.

AU - Prigione, Cristina

AU - Ramos, Fernando A.

AU - Navarro, Sandra M.

AU - Berbotto, Guillermo A.

AU - Jorfen, Marisa

AU - Romero, Elisa J.

AU - Garcia, Mercedes A.

AU - Marcos, Juan C.

AU - Marcos, Ana I.

AU - Perandones, Carlos E.

AU - Eimon, Alicia

AU - Battagliotti, Cristina G.

AU - Armadi-Simab, K.

AU - Gross, Wolfgang L.

AU - Gromnica-Ihle, Erika

AU - Peter, Hans Hartmut

AU - Manger, Karin

AU - Schnarr, Sebastian

AU - Zeidler, Henning

AU - Schmidt, Reinhold E.

AU - Ortego, Norberto

AU - Callejas, José L.

AU - Jiménez-Alonso, Juan

AU - Sabio, Mario

AU - Sánchez-Román, Julio

AU - Garcia-Hernandez, Francisco J.

AU - Camps, Mayte

AU - López-Nevot, Miguel Angel

AU - González-Escribano, Maria F.

AU - Langefeld, Carl

AU - Tsao, Betty

AU - Jacob, Chaim

PY - 2009/4/1

Y1 - 2009/4/1

N2 - Immune-mediated nephritis contributes to disease in systemic lupus erythematosus, Goodpasture syndrome (caused by antibodies specific for glomerular basement membrane [anti-GBM antibodies]), and spontaneous lupus nephritis. Inbred mouse strains differ in susceptibility to anti-GBM antibody-induced and spontaneous lupus nephritis. This study sought to clarify the genetic and molecular factors that may be responsible for enhanced immune-mediated renal disease in these models. When the kidneys of 3 mouse strains sensitive to anti-GBM antibody-induced nephritis were compared with those of 2 control strains using microarray analysis, one-fifth of the underexpressed genes belonged to the kallikrein gene family, which encodes serine esterases. Mouse strains that upregulated renal and urinary kallikreins exhibited less evidence of disease. Antagonizing the kallikrein pathway augmented disease, while agonists dampened the severity of anti-GBM antibody-induced nephritis. In addition, nephritis-sensitive mouse strains had kallikrein haplotypes that were distinct from those of control strains, including several regulatory polymorphisms, some of which were associated with functional consequences. Indeed, increased susceptibility to anti-GBM antibody-induced nephritis and spontaneous lupus nephritis was achieved by breeding mice with a genetic interval harboring the kallikrein genes onto a disease-resistant background. Finally, both human SLE and spontaneous lupus nephritis were found to be associated with kallikrein genes, particularly KLK1 and the KLK3 promoter, when DNA SNPs from independent cohorts of SLE patients and controls were compared. Collectively, these studies suggest that kallikreins are protective disease-associated genes in anti-GBM antibody-induced nephritis and lupus.

AB - Immune-mediated nephritis contributes to disease in systemic lupus erythematosus, Goodpasture syndrome (caused by antibodies specific for glomerular basement membrane [anti-GBM antibodies]), and spontaneous lupus nephritis. Inbred mouse strains differ in susceptibility to anti-GBM antibody-induced and spontaneous lupus nephritis. This study sought to clarify the genetic and molecular factors that may be responsible for enhanced immune-mediated renal disease in these models. When the kidneys of 3 mouse strains sensitive to anti-GBM antibody-induced nephritis were compared with those of 2 control strains using microarray analysis, one-fifth of the underexpressed genes belonged to the kallikrein gene family, which encodes serine esterases. Mouse strains that upregulated renal and urinary kallikreins exhibited less evidence of disease. Antagonizing the kallikrein pathway augmented disease, while agonists dampened the severity of anti-GBM antibody-induced nephritis. In addition, nephritis-sensitive mouse strains had kallikrein haplotypes that were distinct from those of control strains, including several regulatory polymorphisms, some of which were associated with functional consequences. Indeed, increased susceptibility to anti-GBM antibody-induced nephritis and spontaneous lupus nephritis was achieved by breeding mice with a genetic interval harboring the kallikrein genes onto a disease-resistant background. Finally, both human SLE and spontaneous lupus nephritis were found to be associated with kallikrein genes, particularly KLK1 and the KLK3 promoter, when DNA SNPs from independent cohorts of SLE patients and controls were compared. Collectively, these studies suggest that kallikreins are protective disease-associated genes in anti-GBM antibody-induced nephritis and lupus.

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U2 - 10.1172/JCI36728

DO - 10.1172/JCI36728

M3 - Article

C2 - 19307730

AN - SCOPUS:65249086734

VL - 119

SP - 911

EP - 923

JO - Journal of Clinical Investigation

JF - Journal of Clinical Investigation

SN - 0021-9738

IS - 4

ER -