Molecular and bioenergetic differences between cells with African versus European inherited mitochondrial DNA haplogroups: Implications for population susceptibility to diseases

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 2, 2014, Pages 208-219

  Kenney, M Cristina ^a,b   Chwa, Marilyn ^a   Atilano, Shari R ^a   Falatoonzadeh, Payam ^a   Ramirez, Claudio ^a   Malik, Deepika ^a   Tarek, Mohamed ^a   del Carpio, Javier Cáceres ^a   Nesburn, Anthony B ^a,c   Boyer, David S ^d   Kuppermann, Baruch D ^a   Vawter, Marquis P ^b   Jazwinski, S Michal ^e   Miceli, Michael V ^e   Wallace, Douglas C ^f   Udar, Nitin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d RETINA VITREOUS ASSOCIATES MEDICAL GROUP   (United States)

^e TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

Complement activation; Cybrid; Haplogroup; Innate immunity; Mitochondrion; Retina

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHEMOKINE RECEPTOR CCR3; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA2;

AFRICA; ARTICLE; BIOENERGY; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; CYBRID; EUROPE; EXTRACELLULAR SPACE; GENE DOSAGE; GENE EXPRESSION; GENE SEQUENCE; GENETIC SUSCEPTIBILITY; HAPLOTYPE; HUMAN; INNATE IMMUNITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NUCLEOTIDE SEQUENCE; OXYGEN CONSUMPTION; POPULATION GENETICS; PRIORITY JOURNAL;

ABI; ADENOSINE TRIPHOSPHATE; APPLIED BIOSYSTEMS; ARPE-19; ATP; C1S; C3; C4B; CARBONYL CYANIDE 4-TRIFLUOROMETHOXY-PHENYLHYDRAZONE; CFH; COMPLEMENT ACTIVATION; COMPLEMENT COMPONENT 1, S SUBCOMPONENT; COMPLEMENT COMPONENT 3; COMPLEMENT COMPONENT 4B; COMPLEMENT FACTOR H; CYBRID; DEOXYRIBONUCLEIC ACID; DMEM; DNA; DULBECCO'S MODIFIED EAGLE'S MEDIUM; ECAR; EDTA; ELECTRON TRANSPORT CHAIN; ETC; ETHYLENEDIAMINETETRACETIC ACID; EXTRACELLULAR ACIDIFICATION RATE; FCCP; HAPLOGROUP; INNATE IMMUNITY; MAXIMAL OXYGEN UPTAKE; MICROMOLAR; MITOCHONDRIA ENCODED CYTOCHROME B; MITOCHONDRIA ENCODED CYTOCHROME OXIDASE 1; MITOCHONDRIA ENCODED CYTOCHROME OXIDASE 2; MITOCHONDRIA ENCODED CYTOCHROME OXIDASE 3; MITOCHONDRIA ENCODED NADH DEHYDROGENASE 1; MITOCHONDRIA ENCODED NADH DEHYDROGENASE 3; MITOCHONDRIA ENCODED NADH DEHYDROGENASE 5; MITOCHONDRION; MT-CO1; MT-CO2; MT-CO3; MT-CYB; MT-ND1; MT-ND3; MT-ND5; OCR; OXIDATIVE PHOSPHORYLATION; OXPHOS; OXYGEN CONSUMPTION RATE; Q-PCR; QUANTITATIVE POLYMERASE CHAIN REACTION; RETINA; RETINAL PIGMENTED EPITHELIUM CELL LINE; SEM; SINGLE NUCLEOTIDE POLYMORPHISMS; SNPS; STANDARD ERROR MEAN; UCLA; UNIVERSITY OF CALIFORNIA, LOS ANGELES; VO2(MAX); ΜM;

ADENOSINE TRIPHOSPHATE; ADULT; AFRICAN CONTINENTAL ANCESTRY GROUP; CELL LINE; CELL PROLIFERATION; DNA, MITOCHONDRIAL; ENERGY METABOLISM; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENE DOSAGE; GENE EXPRESSION PROFILING; GENES, MITOCHONDRIAL; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; HYBRID CELLS; LACTATES; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84890154942     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.10.016     Document Type: Article

References (81)

1. Wallace D.C., Lott M.T., Procaccio V. Mitochondrial Genes in Degenerative Diseases, Cancer and Aging 2007, Churchill Livingstonr Elsevier, Philadelphis, PA. 5th edition.
2. Wallace D.C. Diseases of the mitochondrial DNA. Annu. Rev. Biochem. 1992, 61:1175-1212.
3. Wallace D.C. Mitochondrial DNA mutations in diseases of energy metabolism. J. Bioenerg. Biomembr. 1994, 26:241-250.
4. McFarland R., Turnbull D.M. Batteries not included: diagnosis and management of mitochondrial disease. J. Intern. Med. 2009, 265:210-228.
5. Bellizzi D., Taverna D., D'Aquila P., De Blasi S., De Benedictis G. Mitochondrial DNA variability modulates mRNA and intra-mitochondrial protein levels of HSP60 and HSP75: experimental evidence from cybrid lines. Cell Stress Chaperones 2009, 14:265-271.
6. Bellizzi D., Cavalcante P., Taverna D., Rose G., Passarino G., Salvioli S., Franceschi C., De Benedictis G. Gene expression of cytokines and cytokine receptors is modulated by the common variability of the mitochondrial DNA in cybrid cell lines. Genes Cells 2006, 11:883-891.
7. Hudson G., Carelli V., Spruijt L., Gerards M., Mowbray C., Achilli A., Pyle A., Elson J., Howell N., La Morgia C., Valentino M.L., Huoponen K., Savontaus M.L., Nikoskelainen E., Sadun A.A., Salomao S.R., Belfort R., Griffiths P., Man P.Y., de Coo R.F., Horvath R., Zeviani M., Smeets H.J., Torroni A., Chinnery P.F. Clinical expression of Leber hereditary optic neuropathy is affected by the mitochondrial DNA-haplogroup background. Am. J. Hum. Genet. 2007, 81:228-233.
8. Strauss K.A., DuBiner L., Simon M., Zaragoza M., Sengupta P.P., Li P., Narula N., Dreike S., Platt J., Procaccio V., Ortiz-Gonzalez X.R., Puffenberger E.G., Kelley R.I., Morton D.H., Narula J., Wallace D.C. Severity of cardiomyopathy associated with adenine nucleotide translocator-1 deficiency correlates with mtDNA haplogroup. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:3453-3458.
9. van der Walt J.M., Dementieva Y.A., Martin E.R., Scott W.K., Nicodemus K.K., Kroner C.C., Welsh-Bohmer K.A., Saunders A.M., Roses A.D., Small G.W., Schmechel D.E., Murali Doraiswamy P., Gilbert J.R., Haines J.L., Vance J.M., Pericak-Vance M.A. Analysis of European mitochondrial haplogroups with Alzheimer disease risk. Neurosci. Lett. 2004, 365:28-32.
10. van der Walt J.M., Nicodemus K.K., Martin E.R., Scott W.K., Nance M.A., Watts R.L., Hubble J.P., Haines J.L., Koller W.C., Lyons K., Pahwa R., Stern M.B., Colcher A., Hiner B.C., Jankovic J., Ondo W.G., Allen F.H., Goetz C.G., Small G.W., Mastaglia F., Stajich J.M., McLaurin A.C., Middleton L.T., Scott B.L., Schmechel D.E., Pericak-Vance M.A., Vance J.M. Mitochondrial polymorphisms significantly reduce the risk of Parkinson disease. Am. J. Hum. Genet. 2003, 72:804-811.
11. Huerta C., Castro M.G., Coto E., Blazquez M., Ribacoba R., Guisasola L.M., Salvador C., Martinez C., Lahoz C.H., Alvarez V. Mitochondrial DNA polymorphisms and risk of Parkinson's disease in Spanish population. J. Neurol. Sci. 2005, 236:49-54.
12. Coskun P., Wyrembak J., Schriner S., Chen H.W., Marciniack C., Laferla F., Wallace D.C. A mitochondrial etiology of Alzheimer and Parkinson disease. Biochim. Biophys. Acta 2012, 1820:553-564.
13. Fernandez-Moreno M., Soto-Hermida A., Oreiro N., Pertega S., Fenandez-Lopez C., Rego-Perez I., Blanco F.J. Mitochondrial haplogroups define two phenotypes of osteoarthritis. Front. Physiol. 2012, 3:129.
14. Achilli A., Olivieri A., Pala M., Hooshiar Kashani B., Carossa V., Perego U.A., Gandini F., Santoro A., Battaglia V., Grugni V., Lancioni H., Sirolla C., Bonfigli A.R., Cormio A., Boemi M., Testa I., Semino O., Ceriello A., Spazzafumo L., Gadaleta M.N., Marra M., Testa R., Franceschi C., Torroni A. Mitochondrial DNA backgrounds might modulate diabetes complications rather than T2DM as a whole. PLoS ONE 2011, 6:e21029.
15. Czarnecka A.M., Bartnik E. The role of the mitochondrial genome in ageing and carcinogenesis. J. Aging Res. 2011, 136435.
16. Hatzfeld J.J., LaVeist T.A., Gaston-Johansson F.G. Racial/ethnic disparities in the prevalence of selected chronic diseases among US Air Force members, 2008. Prev. Chronic Dis. 2012, 9:E112.
17. Mensah G.A., Mokdad A.H., Ford E.S., Greenlund K.J., Croft J.B. State of disparities in cardiovascular health in the United States. Circulation 2005, 111:1233-1241.
18. Kurian A.K., Cardarelli K.M. Racial and ethnic differences in cardiovascular disease risk factors: a systematic review. Ethn. Dis. 2007, 17:143-152.
19. Peek M.E., Cargill A., Huang E.S. Diabetes health disparities: a systematic review of health care interventions. Med. Care Res. Rev. 2007, 64:101S-156S.
20. Feldman C.H., Hiraki L.T., Liu J., Fischer M.A., Solomon D.H., Alarcon G.S., Winkelmayer W.C., Costenbader K.H. Epidemiology and sociodemographics of systemic lupus erythematosus and lupus nephritis among US adults with Medicaid coverage, 2000-2004. Arthritis Rheum. 2013, 65:753-763.
21. Hiraki L.T., Feldman C.H., Liu J., Alarcon G.S., Fischer M.A., Winkelmayer W.C., Costenbader K.H. Prevalence, incidence, and demographics of systemic lupus erythematosus and lupus nephritis from 2000 to 2004 among children in the US Medicaid beneficiary population. Arthritis Rheum. 2012, 64:2669-2676.
22. Manly JJ M.R. Ethnic Differences in Dementia and Alzheimer's Disease 2004, Natl Acad Press, Washington, DC.
23. Dilworth-Anderson P., Hendrie H.C., Manly J.J., Khachaturian A.S., Fazio S. Diagnosis and assessment of Alzheimer's disease in diverse populations. Alzheimers Dement. 2008, 4:305-309.
24. Potter G.G., Plassman B.L., Burke J.R., Kabeto M.U., Langa K.M., Llewellyn D.J., Rogers M.A., Steffens D.C. Cognitive performance and informant reports in the diagnosis of cognitive impairment and dementia in African Americans and whites. Alzheimers Dement. 2009, 5:445-453.
25. Wiley K.L., Treadwell E., Manigaba K., Word B., Lyn-Cook B.D. Ethnic differences in DNA methyltransferases expression in patients with systemic lupus erythematosus. J. Clin. Immunol. 2013, 33:342-348.
26. Gomez-Duran A., Pacheu-Grau D., Martinez-Romero I., Lopez-Gallardo E., Lopez-Perez M.J., Montoya J., Ruiz-Pesini E. Oxidative phosphorylation differences between mitochondrial DNA haplogroups modify the risk of Leber's hereditary optic neuropathy. Biochim. Biophys. Acta 2012, 1822:1216-1222.
27. Miceli M.V., Jazwinski S.M. Nuclear gene expression changes due to mitochondrial dysfunction in ARPE-19 cells: implications for age-related macular degeneration. Inves. Ophthalmol. Vis. Sci. 2005, 46:1765-1773.
28. Chomyn A. Platelet-mediated Transformation of Human Mitochondrial DNA-less Cells 1996, Academic Press, Inc., Salt Lake City, UT.
29. Udar N., Atilano S.R., Memarzadeh M., Boyer D., Chwa M., Lu S., Maguen B., Langberg J., Coskun P., Wallace D.C., Nesburn A.B., Khatibi N., Hertzog D., Le K., Hwang D.W., Kenney M.C. Mitochondrial DNA haplogroups associated with age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2009, 50:2966-2974.
30. Kenney M.C., Chwa M., Atilano S.R., Pavlis J.M., Falatoonzadeh P., Ramirez C., Malik D., Hsu T., Woo G., Soe K., Nesburn A.B., Boyer D.S., Kuppermann B.D., Jazwinski S.M., Miceli M.V., Wallace D.C., Udar N. Mitochondrial DNA variants mediate energy production and expression levels for CFH, C3, and EFEMP1 genes: implications for age-related macular degeneration. PLoS ONE 2013, 8:e54339-e54348.
31. Scott R.A., Fuku N., Onywera V.O., Boit M., Wilson R.H., Tanaka M., W H.G., Pitsiladis Y.P., H.G.W., Pitsiladis Y.P. Mitochondrial haplogroups associated with elite Kenyan athlete status. Med. Sci. Sports Exerc. 2009, 41:123-128.
32. Scott R.A., Wilson R.H., Goodwin W.H., Moran C.N., Georgiades E., Wolde B., Pitsiladis Y.P. Mitochondrial DNA lineages of elite Ethiopian athletes. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2005, 140:497-503.
33. Schnabelrauch M., Scharnweber D., Schiller J. Sulfated glycosaminoglycans as promising artificial extracellular matrix components to improve the regeneration of tissues. Curr. Med. Chem. 2013, 20:2501-2523.
34. Rho J.H., Zhang W., Murali M., Roehrl M.H., Wang J.Y. Human proteins with affinity for dermatan sulfate have the propensity to become autoantigens. Am. J. Pathol. 2011, 178:2177-2190.
35. Hansen C., Otto E., Kuhlemann K., Forster G., Kahaly G.J. Glycosaminoglycans in autoimmunity. Clin. Exp. Rheumatol. 1996, 14(Suppl. 15):S59-S67.
36. De Muro P., Faedda R., Formato M., Re F., Satta A., Cherchi G.M., Carcassi A. Urinary glycosaminoglycans in patients with systemic lupus erythematosus. Clin. Exp. Rheumatol. 2001, 19:125-130.
37. Campo G.M., Avenoso A., Campo S., D'Ascola A., Traina P., Sama D., Calatroni A. Purified human plasma glycosaminoglycans reduced NF-kappaB activation, pro-inflammatory cytokine production and apoptosis in LPS-treated chondrocytes. Innate Immun. 2008, 14:233-246.
38. Haylock-Jacobs S., Keough M.B., Lau L., Yong V.W. Chondroitin sulphate proteoglycans: extracellular matrix proteins that regulate immunity of the central nervous system. Autoimmun. Rev. 2011, 10:766-772.
39. Vallieres M., du Souich P. Modulation of inflammation by chondroitin sulfate. Osteoarthritis Cartilage 2010, 18(Suppl. 1):S1-S6.
40. du Souich P., Garcia A.G., Verges J., Montell E. Immunomodulatory and anti-inflammatory effects of chondroitin sulphate. J. Cell. Mol. Med. 2009, 13:1451-1463.
41. Egea J., Garcia A.G., Verges J., Montell E., Lopez M.G. Antioxidant, antiinflammatory and neuroprotective actions of chondroitin sulfate and proteoglycans. Osteoarthritis Cartilage 2010, 18(Suppl. 1):S24-S27.
42. Mizumoto S., Ikegawa S., Sugahara K. Human genetic disorders caused by mutations in genes encoding biosynthetic enzymes for sulfated glycosaminoglycans. J. Biol. Chem. 2013, 288:10953-10961.
43. Weiser P., Qian Y., Pan J., Zhou X., Lu H., Studelska D.R., Shih F.F., Zhang L. Activated contact system and abnormal glycosaminoglycans in lupus and other auto- and non-autoimmune diseases. Prog. Mol. Biol. Transl. Sci. 2010, 93:443-472.
44. Robson M.G., Walport M.J. Pathogenesis of systemic lupus erythematosus (SLE). Clin. Exp. Allergy 2001, 31:678-685.
45. Lood C., Gullstrand B., Truedsson L., Olin A.I., Alm G.V., Ronnblom L., Sturfelt G., Eloranta M.L., Bengtsson A.A. C1q inhibits immune complex-induced interferon-alpha production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum. 2009, 60:3081-3090.
46. Inoue N., Saito T., Masuda R., Suzuki Y., Ohtomi M., Sakiyama H. Selective complement C1s deficiency caused by homozygous four-base deletion in the C1s gene. Hum. Genet. 1998, 103:415-418.
47. Ohno-Matsui K. Parallel findings in age-related macular degeneration and Alzheimer's disease. Prog. Retin. Eye Res. 2011, 30:217-238.
48. Moreno-Navarrete J.M., Martinez-Barricarte R., Catalan V., Sabater M., Gomez-Ambrosi J., Ortega F.J., Ricart W., Bluher M., Fruhbeck G., Rodriguez de Cordoba S., Fernandez-Real J.M. Complement factor H is expressed in adipose tissue in association with insulin resistance. Diabetes 2010, 59:200-209.
49. Fujita T., Hemmi S., Kajiwara M., Yabuki M., Fuke Y., Satomura A., Soma M. Complement-mediated chronic inflammation is associated with diabetic microvascular complication. Diabetes Metab. Res. Rev. 2013, 29:220-226.
50. Ferreira I.L., Nascimento M.V., Ribeiro M., Almeida S., Cardoso S.M., Grazina M., Pratas J., Santos M.J., Januario C., Oliveira C.R., Rego A.C. Mitochondrial-dependent apoptosis in Huntington's disease human cybrids. Exp. Neurol. 2010, 222:243-255.
51. Jun A.S., Trounce I.A., Brown M.D., Shoffner J.M., Wallace D.C. Use of transmitochondrial cybrids to assign a complex I defect to the mitochondrial DNA-encoded NADH dehydrogenase subunit 6 gene mutation at nucleotide pair 14459 that causes Leber hereditary optic neuropathy and dystonia. Mol. Cell. Biol. 1996, 16:771-777.
52. Brown M.D., Trounce I.A., Jun A.S., Allen J.C., Wallace D.C. Functional analysis of lymphoblast and cybrid mitochondria containing the 3460, 11778, or 14484 Leber's hereditary optic neuropathy mitochondrial DNA mutation. J. Biol. Chem. 2000, 275:39831-39836.
53. Arning L., Haghikia A., Taherzadeh-Fard E., Saft C., Andrich J., Pula B., Hoxtermann S., Wieczorek S., Akkad D.A., Perrech M., Gold R., Epplen J.T., Chan A. Mitochondrial haplogroup H correlates with ATP levels and age at onset in Huntington disease. J. Mol. Med. 2010, 88:431-436.
54. Murphy G.E., Xu D., Liew F.Y., McInnes I.B. Role of interleukin 33 in human immunopathology. Ann. Rheum. Dis. 2010, 69(Suppl. 1):i43-i47.
55. Liew F.Y. IL-33: a Janus cytokine. Ann. Rheum. Dis. 2012, 71(Suppl. 2):i101-i104.
56. Kuchler A.M., Pollheimer J., Balogh J., Sponheim J., Manley L., Sorensen D.R., De Angelis P.M., Scott H., Haraldsen G. Nuclear interleukin-33 is generally expressed in resting endothelium but rapidly lost upon angiogenic or proinflammatory activation. Am. J. Pathol. 2008, 173:1229-1242.
57. Miller A.M., Xu D., Asquith D.L., Denby L., Li Y., Sattar N., Baker A.H., McInnes I.B., Liew F.Y. IL-33 reduces the development of atherosclerosis. J. Exp. Med. 2008, 205:339-346.
58. Rank M.A., Kobayashi T., Kozaki H., Bartemes K.R., Squillace D.L., Kita H. IL-33-activated dendritic cells induce an atypical TH2-type response. J. Allergy Clin. Immunol. 2009, 123:1047-1054.
59. Carriere V., Roussel L., Ortega N., Lacorre D.A., Americh L., Aguilar L., Bouche G., Girard J.P. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:282-287.
60. Leung B.P., Xu D., Culshaw S., McInnes I.B., Liew F.Y. A novel therapy of murine collagen-induced arthritis with soluble T1/ST2. J. Immunol. 2004, 173:145-150.
61. Seidelin J.B., Bjerrum J.T., Coskun M., Widjaya B., Vainer B., Nielsen O.H. IL-33 is upregulated in colonocytes of ulcerative colitis. Immunol. Lett. 2010, 128:80-85.
62. Kurowska-Stolarska M., Stolarski B., Kewin P., Murphy G., Corrigan C.J., Ying S., Pitman N., Mirchandani A., Rana B., van Rooijen N., Shepherd M., McSharry C., McInnes I.B., Xu D., Liew F.Y. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J. Immunol. 2009, 183:6469-6477.
63. Schmitz J., Owyang A., Oldham E., Song Y., Murphy E., McClanahan T.K., Zurawski G., Moshrefi M., Qin J., Li X., Gorman D.M., Bazan J.F., Kastelein R.A. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005, 23:479-490.
64. Smithgall M.D., Comeau M.R., Yoon B.R., Kaufman D., Armitage R., Smith D.E. IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int. Immunol. 2008, 20:1019-1030.
65. Komai-Koma M., Xu D., Li Y., McKenzie A.N., McInnes I.B., Liew F.Y. IL-33 is a chemoattractant for human Th2 cells. Eur. J. Immunol. 2007, 37:2779-2786.
66. Mirchandani A.S., Salmond R.J., Liew F.Y. Interleukin-33 and the function of innate lymphoid cells. Trends Immunol. 2012, 33:389-396.
67. Milovanovic M., Volarevic V., Radosavljevic G., Jovanovic I., Pejnovic N., Arsenijevic N., Lukic M.L. IL-33/ST2 axis in inflammation and immunopathology. Immunol. Res. 2012, 52:89-99.
68. Ali S., Mohs A., Thomas M., Klare J., Ross R., Schmitz M.L., Martin M.U. The dual function cytokine IL-33 interacts with the transcription factor NF-kappaB to dampen NF-kappaB-stimulated gene transcription. J. Immunol. 2011, 187:1609-1616.
69. Lillien L., Cepko C. Control of proliferation in the retina: temporal changes in responsiveness to FGF and TGF alpha. Development 1992, 115:253-266.
70. Sagar S.M., Edwards R.H., Sharp F.R. Epidermal growth factor and transforming growth factor alpha induce c-fos gene expression in retinal Muller cells in vivo. J. Neurosci. Res. 1991, 29:549-559.
71. Fassio J.B., Brockman E.B., Jumblatt M., Greaton C., Henry J.L., Geoghegan T.E., Barr C., Schultz G.S. Transforming growth factor alpha and its receptor in neural retina. Invest. Ophthalmol. Vis. Sci. 1989, 30:1916-1922.
72. Brissenden J.E., Derynck R., Francke U. Mapping of transforming growth factor alpha gene on human chromosome 2 close to the breakpoint of the Burkitt's lymphoma t(2;8) variant translocation. Cancer Res. 1985, 45:5593-5597.
73. Ellis D.L., Kafka S.P., Chow J.C., Nanney L.B., Inman W.H., McCadden M.E., King L.E. Melanoma, growth factors, acanthosis nigricans, the sign of Leser-Trelat, and multiple acrochordons. A possible role for alpha-transforming growth factor in cutaneous paraneoplastic syndromes. N. Engl. J. Med. 1987, 317:1582-1587.
74. Letra A., Fakhouri W., Fonseca R.F., Menezes R., Kempa I., Prasad J.L., McHenry T.G., Lidral A.C., Moreno L., Murray J.C., Daack-Hirsch S., Marazita M.L., Castilla E.E., Lace B., Orioli I.M., Granjeiro J.M., Schutte B.C., Vieira A.R. Interaction between IRF6 and TGFA genes contribute to the risk of nonsyndromic cleft lip/palate. PLoS ONE 2012, 7:e45441.
75. Vieira A.R. Association between the transforming growth factor alpha gene and nonsyndromic oral clefts: a HuGE review. Am. J. Epidemiol. 2006, 163:790-810.
76. Vollebergh M.A., Kappers I., Klomp H.M., Buning-Kager J.C., Korse C.M., Hauptmann M., de Visser K.E., van den Heuvel M.M., Linn S.C. Ligands of epidermal growth factor receptor and the insulin-like growth factor family as serum biomarkers for response to epidermal growth factor receptor inhibitors in patients with advanced non-small cell lung cancer. J. Thorac. Oncol. 2010, 5:1939-1948.
77. Kramer A., Yang F.C., Snodgrass P., Li X., Scammell T.E., Davis F.C., Weitz C.J. Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 2001, 294:2511-2515.
78. Resnick L., Fennell M. Targeting JNK3 for the treatment of neurodegenerative disorders. Drug Discov. Today 2004, 9:932-939.
79. Abdelli S., Puyal J., Bielmann C., Buchillier V., Abderrahmani A., Clarke P.G., Beckmann J.S., Bonny C. JNK3 is abundant in insulin-secreting cells and protects against cytokine-induced apoptosis. Diabetologia 2009, 52:1871-1880.
80. Yoon S.O., Park D.J., Ryu J.C., Ozer H.G., Tep C., Shin Y.J., Lim T.H., Pastorino L., Kunwar A.J., Walton J.C., Nagahara A.H., Lu K.P., Nelson R.J., Tuszynski M.H., Huang K. JNK3 perpetuates metabolic stress induced by Abeta peptides. Neuron 2012, 75:824-837.
81. Fernandes K.A., Harder J.M., Fornarola L.B., Freeman R.S., Clark A.F., Pang I.H., John S.W., Libby R.T. JNK2 and JNK3 are major regulators of axonal injury-induced retinal ganglion cell death. Neurobiol. Dis. 2012, 46:393-401.