Loss of epithelial membrane protein 2 aggravates podocyte injury via upregulation of caveolin-1

Journal of the American Society of Nephrology

Volumn 27, Issue 4, 2016, Pages 1066-1075

  Wan, Xiaoyang ^a   Chen, Zhaohong ^a,b   Choi, Won Il ^c   Gee, Heon Yung ^c   Hildebrandt, Friedhelm ^c,d   Zhou, Weibin ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b JINLING HOSPITAL   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CAVEOLIN 1; DEXAMETHASONE; EPITHELIAL MEMBRANE PROTEIN 2; MEMBRANE PROTEIN; PREDNISONE; PUROMYCIN AMINONUCLEOSIDE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; EMP2 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CAVEOLA; CELL DAMAGE; CELL SURVIVAL; CONTROLLED STUDY; DELETION MUTANT; DISEASE EXACERBATION; DOWN REGULATION; EMBRYO; EXPERIMENTAL MODEL; GENE EDITING; GENE OVEREXPRESSION; HOMOZYGOTE; HUMAN; HUMAN CELL; NEPHROTIC SYNDROME; NONHUMAN; ORBIT EDEMA; PATHOGENESIS; PERIORBITAL EDEMA; PHENOTYPE; PODOCYTE; PRIORITY JOURNAL; PROTEINURIA; QUANTITATIVE ANALYSIS; UPREGULATION; ZEBRA FISH; ANIMAL; PHYSIOLOGY;

ANIMALS; CAVEOLIN 1; HUMANS; MEMBRANE GLYCOPROTEINS; NEPHROTIC SYNDROME; PODOCYTES; UP-REGULATION; ZEBRAFISH;

EID: 85017049440     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014121197     Document Type: Article

References (40)

1. Lane JC, Kaskel FJ: Pediatric nephrotic syndrome: From the simple to the complex. Semin Nephrol 29: 389–398, 2009
2. Abeyagunawardena AS: Treatment of steroid sensitive nephrotic syndrome. Indian J Pediatr 72: 763–769, 2005
3. Gee HY, Ashraf S, Wan X, Vega-Warner V, Esteve-Rudd J, Lovric S, Fang H, Hurd TW, Sadowski CE, Allen SJ, Otto EA, Korkmaz E, Washburn J, Levy S, Williams DS, Bakkaloglu SA, Zolotnitskaya A, Ozaltin F, Zhou W, Hildebrandt F: Mutations in EMP2 cause childhood-onset nephrotic syndrome. Am J Hum Genet 94: 884–890, 2014
4. Wadehra M, Iyer R, Goodglick L, Braun J: The tetraspan protein epithelial membrane protein-2 interacts with beta1 integrins and regulates adhesion. J Biol Chem 277: 41094–41100, 2002
5. Wadehra M, Goodglick L, Braun J: The tetraspan protein EMP2 modulates the surface expression of caveolins and glycosylphosphatidyl inositol-linked proteins. Mol Biol Cell 15: 2073–2083, 2004
6. Forbes A, Wadehra M, Mareninov S, Morales S, Shimazaki K, Gordon LK, Braun J: The tetraspan protein EMP2 regulates expression of caveolin-1. J Biol Chem 282: 26542–26551, 2007
7. Zhou W, Hildebrandt F: Inducible podocyte injury and proteinuria in transgenic zebrafish. J Am Soc Nephrol 23: 1039–1047, 2012
8. Curado S, Stainier DY, Anderson RM: Nitroreductase-mediated cell/ tissue ablation in zebrafish: A spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat Protoc 3: 948–954, 2008
9. Pisharath H, Parsons MJ: Nitroreductase-mediated cell ablation in transgenic zebrafish embryos. Methods Mol Biol 546: 133–143, 2009
10. Rossmann P, Bukovský A, Matousovic K, Holub M, Král J: Puromycin aminonucleoside nephropathy: Ultrastructure, glomerular polyanion, and cell surface markers. J Pathol 148: 337–348, 1986
11. Moriyama T, Tsuruta Y, Shimizu A, Itabashi M, Takei T, Horita S, Uchida K, Nitta K: The significance of caveolae in the glomeruli in glomerular disease. J Clin Pathol 64: 504–509, 2011
12. Nykjaer A, Fyfe JC, Kozyraki R, Leheste JR, Jacobsen C, Nielsen MS, Verroust PJ, Aminoff M, de la Chapelle A, Moestrup SK, Ray R, Gliemann J, Willnow TE, Christensen EI: Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D(3). Proc Natl Acad Sci U S A 98: 13895–13900, 2001
13. Anzenberger U, Bit-Avragim N, Rohr S, Rudolph F, Dehmel B, Willnow TE, Abdelilah-Seyfried S: Elucidation of megalin/LRP2-dependent endocytic transport processes in the larval zebrafish pronephros. J Cell Sci 119: 2127–2137, 2006
14. Gvaramia D, Blaauboer ME, Hanemaaijer R, Everts V: Role of caveolin-1 in fibrotic diseases. Matrix Biol 32: 307–315, 2013
15. Sörensson J, Fierlbeck W, Heider T, Schwarz K, Park DS, Mundel P, Lisanti M, Ballermann BJ: Glomerular endothelial fenestrae in vivo are not formed from caveolae. J Am Soc Nephrol 13: 2639–2647, 2002
16. Ren Z, Liang W, Chen C, Yang H, Singhal PC, Ding G: Angiotensin II induces nephrin dephosphorylation and podocyte injury: Role of caveolin-1. Cell Signal 24: 443–450, 2012
17. Bartholomew JN, Volonte D, Galbiati F: Caveolin-1 regulates the antagonistic pleiotropic properties of cellular senescence through a novel Mdm2/p53-mediated pathway. Cancer Res 69: 2878–2886, 2009
18. Volonte D, Zhang K, Lisanti MP, Galbiati F: Expression of caveolin-1 induces premature cellular senescence in primary cultures of murine fibroblasts. Mol Biol Cell 13: 2502–2517, 2002
19. Zou H, Stoppani E, Volonte D, Galbiati F: Caveolin-1, cellular senescence and age-related diseases. Mech Ageing Dev 132: 533–542, 2011
20. Bitar MS, Abdel-Halim SM, Al-Mulla F: Caveolin-1/PTRF upregulation constitutes a mechanism for mediating p53-induced cellular senescence: Implications for evidence-based therapy of delayed wound healing in diabetes. Am J Physiol Endocrinol Metab 305: E951–E963, 2013
21. Thomasova D, Bruns HA, Kretschmer V, Ebrahim M, Romoli S, Liapis H, Kotb AM, Endlich N, Anders HJ: Murine double minute-2 prevents p53-overactivation-related cell death (podoptosis) of podocytes. J Am Soc Nephrol 26: 1513–1523, 2015
22. Mulay SR, Thomasova D, Ryu M, Kulkarni OP, Migliorini A, Bruns H, Gröbmayr R, Lazzeri E, Lasagni L, Liapis H, Romagnani P, Anders HJ: Podocyte loss involves MDM2-driven mitotic catastrophe. J Pathol 230: 322–335, 2013
23. Ingueneau C, Huynh UD, Marcheix B, Athias A, Gambert P, Nègre-Salvayre A, Salvayre R, Vindis C: TRPC1 is regulated by caveolin-1 and is involved in oxidized LDL-induced apoptosis of vascular smooth muscle cells. J Cell Mol Med 13: 1620–1631, 2009
24. Yeh YC, Parekh AB: Distinct structural domains of caveolin-1 independently regulate Ca2+ release-activated Ca2+ channels and Ca2 + microdomain-dependent gene expression. Mol Cell Biol 35: 1341–1349, 2015
25. Yeh YC, Tang MJ, Parekh AB: Caveolin-1 alters the pattern of cytoplasmic Ca2+ oscillations and Ca2+-dependent gene expression by enhancing leukotriene receptor desensitization. J Biol Chem 289: 17843–17853, 2014
26. Yu S, Li Y: Dexamethasone inhibits podocyte apoptosis by stabilizing the PI3K/Akt signal pathway. BioMed Res Int 326986: 2013, 2013
27. Wu J, Zheng C, Fan Y, Zeng C, Chen Z, Qin W, Zhang C, Zhang W, Wang X, Zhu X, Zhang M, Zen K, Liu Z: Downregulation of microRNA-30 facilitates podocyte injury and is prevented by glucocorticoids. J Am Soc Nephrol 25: 92–104, 2014
28. Yu M, Ren Q, Yu SY: Role of nephrin phosphorylation inducted by dexamethasone and angiotensin II in podocytes. Mol Biol Rep 41: 3591–3595, 2014
29. Hnasko R, Lisanti MP: The biology of caveolae: Lessons from caveolin knockout mice and implications for human disease. Mol Interv 3: 445–464, 2003
30. Guan TH, Chen G, Gao B, Janssen MR, Uttarwar L, Ingram AJ, Krepinsky JC: Caveolin-1 deficiency protects against mesangial matrix expansion in a mouse model of type 1 diabetic nephropathy. Diabetologia 56: 2068–2077, 2013
31. Morales SA, Mareninov S, Wadehra M, Zhang L, Goodglick L, Braun J, Gordon LK: FAK activation and the role of epithelial membrane protein 2 (EMP2) in collagen gel contraction. Invest Ophthalmol Vis Sci 50: 462–469, 2009
32. Qin Y, Fu M, Takahashi M, Iwanami A, Kuga D, Rao RG, Sudhakar D, Huang T, Kiyohara M, Torres K, Dillard C, Inagaki A, Kasahara N, Goodglick L, Braun J, Mischel PS, Gordon LK, Wadehra M: Epithelial membrane protein-2 (EMP2) activates Src protein and is a novel therapeutic target for glioblastoma. J Biol Chem 289: 13974–13985, 2014
33. Reyon D, Maeder ML, Khayter C, Tsai SQ, Foley JE, Sander JD, Joung JK: Engineering customized TALE nucleases (TALENs) and TALE transcription factors by fast ligation-based automatable solid-phase high-throughput (FLASH) assembly. Curr Protoc Mol Biol Chapter 12: Unit 12. 16, 2013
34. Davison JM, Akitake CM, Goll MG, Rhee JM, Gosse N, Baier H, Halpern ME, Leach SD, Parsons MJ: Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Dev Biol 304: 811–824, 2007
35. Zhou W, Boucher RC, Bollig F, Englert C, Hildebrandt F: Characterization of mesonephric development and regeneration using transgenic zebrafish. Am J Physiol Renal Physiol 299: F1040–F1047, 2010
36. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB: The Tol2kit: A multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236: 3088–3099, 2007
37. Fang PK, Solomon KR, Zhuang L, Qi M, McKee M, Freeman MR, Yelick PC: Caveolin-1alpha and -1beta perform nonredundant roles in early vertebrate development. Am J Pathol 169: 2209–2222, 2006
38. Thisse C, Thisse B: High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 3: 59–69, 2008
39. Gee HY, Tang BL, Kim KH, Lee MG: Syntaxin 16 binds to cystic fibrosis transmembrane conductance regulator and regulates its membrane trafficking in epithelial cells. J Biol Chem 285: 35519–35527, 2010
40. Kramer-Zucker AG, Wiessner S, Jensen AM, Drummond IA: Organization of the pronephric filtration apparatus in zebrafish requires Nephrin, Podocin and the FERM domain protein Mosaic eyes. Dev Biol 285: 316–329, 2005