REEP1 mutations in SPG31: Frequency, mutational spectrum, and potential association with mitochondrial morpho-functional dysfunction

Human Mutation

Volumn 32, Issue 10, 2011, Pages 1118-1127

  Goizet, Cyril ^a,b,c,d,f   Depienne, Christel ^b,c,d,e   Benard, Giovanni ^a   Boukhris, Amir ^b,c,d,e,g   Mundwiller, Emeline ^b,c,d   Solé, Guilhem ^a,f   Coupry, Isabelle ^a   Pilliod, Julie ^a   Martin Négrier, Marie Laure ^f   Fedirko, Estelle ^e   Forlani, Sylvie ^b,c,d   Cazeneuve, Cécile ^e   Hannequin, Didier ^h   Charles, Perrine ^e   Feki, Imed ^b,c,g   Pinel, Jean François ⁱ   Ouvrard Hernandez, Anne Marie ^j   Lyonnet, Stanislas ^k   Ollagnon Roman, Elisabeth ^l   Yaouanq, Jacqueline ⁱ   Toutain, Annick ^m   Dussert, Christelle ^b,c,d   Fontaine, Bertrand ^b,c,d,e   Leguern, Eric ^b,c,d,e   Lacombe, Didier ^a,f   Durr, Alexandra ^b,c,d,e   Rossignol, Rodrigue ^a   Brice, Alexis ^b,c,d,e   Stevanin, Giovanni ^b,c,d,e,n   more..

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSERM   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d CNRS   (France)

^e ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^f BORDEAUX UNIVERSITY HOSPITAL   (France)

^g HABIB BOURGUIBA HOSPITAL   (Tunisia)

^h ROUEN UNIVERSITY HOSPITAL   (France)

ⁱ PONTCHAILLOU UNIVERSITY HOSPITAL   (France)

^j GRENOBLE UNIVERSITY HOSPITAL   (France)

^k UNIVERSITÉ PARIS DESCARTES   (France)

^l CROIX ROUSSE HOSPITAL   (France)

^m UNIVERSITY HOSPITAL OF TOURS   (France)

ⁿ PSL RESEARCH UNIVERSITY   (France)

more..

Author keywords

Hereditary spastic paraplegia; Mitochondria; Mitochondrial network; REEP1; SPG31

Indexed keywords

ADOLESCENT; ADULT; AGED; ARTICLE; CEREBELLAR ATAXIA; CHILD; DEMENTIA; FEMALE; GENE; GENE DELETION; GENE MUTATION; GENE REARRANGEMENT; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; NEWBORN; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PYRAMIDAL SIGN; REEP1 GENE; SPG31 GENE; TREMOR;

ADOLESCENT; ADULT; AGED; BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; ENERGY METABOLISM; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; MALE; MEMBRANE TRANSPORT PROTEINS; MIDDLE AGED; MITOCHONDRIA; MUSCLE, SKELETAL; MUTATION; MUTATION RATE; PEDIGREE; PHENOTYPE; SEQUENCE DELETION; SPASTIC PARAPLEGIA, HEREDITARY; YOUNG ADULT;

EID: 80053020946     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.21542     Document Type: Article

References (55)

1. Arnoldi A, Tonelli A, Crippa F, Villani G, Pacelli C, Sironi M, Pozzoli U, D'Angelo MG, Meola G, Martinuzzi A, Crimella C, Redaelli F, Panzeri C, Renieri A, Comi GP, Turconi AC, Bresolin N, Bassi MT. 2008. A clinical, genetic, and biochemical characterization of SPG7 mutations in a large cohort of patients with hereditary spastic paraplegia. Hum Mutat 29:522-531.
2. Atorino L, Silvestri L, Koppen M, Cassina L, Ballabio A, Marconi R, Langer T, Casari G. 2003. Loss of m-AAA protease in mitochondria causes complex I deficiency and increased sensitivity to oxidative stress in hereditary spastic paraplegia. J Cell Biol 163:777-787.
3. Battini R, Fogli A, Borghetti D, Michelucci A, Perazza S, Baldinotti F, Conidi ME, Ferreri MI, Simi P, Cioni G. 2011. Clinical and genetic findings in a series of Italian children with pure hereditary spastic paraplegia. Eur J Neurol 18:150-157.
4. Baxter RV, Ben Othmane K, Rochelle JM, Stajich JE, Hulette C, Dew-Knight S, Hentati F, Ben Hamida M, Bel S, Stenger JE, Gilbert JR, Pericak-Vance MA, Vance JM. 2002. Ganglioside-induced differentiation-associated protein-1 is mutant in Charcot-Marie-Tooth disease type 4A/8q21. Nat Genet 30:21-22.
5. Beetz C, Schule R, Deconinck T, Tran-Viet KN, Zhu H, Kremer BP, Frints SG, van Zelst-Stams WA, Byrne P, Otto S, Nygren AO, Baets J, Smets K, Ceulemans B, Dan B, Nagan N, Kassubek J, Klimpe S, Klopstock T, Stolze H, Smeets HJ, Schrander-Stumpel CT, Hutchinson M, van de Warrenburg BP, Braastad C, Deufel T, Pericak-Vance M, Schols L, de Jonghe P, Zuchner S. 2008. REEP1 mutation spectrum and genotype/phenotype correlation in hereditary spastic paraplegia type 31. Brain 131:1078-1086.
6. Behan WM, Maia M. 1974. Strumpell's familial spastic paraplegia: genetics and neuropathology. J Neurol Neurosurg Psychiatry 37:8-20.
7. Behrens M, Bartelt J, Reichling C, Winnig M, Kuhn C, Meyerhof W. 2006. Members of RTP and REEP gene families influence functional bitter taste receptor expression. J Biol Chem 281:20650-20659.
8. Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T, Rossignol R. 2007. Mitochondrial bioenergetics and structural network organization. J Cell Sci 120:838-848.
9. Bruyn RP. 1992. The neuropathology of hereditary spastic paraparesis. Clin Neurol Neurosurg 94 Suppl:S16-S18.
10. Cartegni L, Chew SL, Krainer AR. 2002. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet 3:285-298.
11. Casari G, De Fusco M, Ciarmatori S, Zeviani M, Mora M, Fernandez P, De Michele G, Filla A, Cocozza S, Marconi R, Durr A, Fontaine B, Ballabio A. 1998. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 93:973-983.
12. Cassereau J, Chevrollier A, Gueguen N, Malinge MC, Letournel F, Nicolas G, Richard L, Ferre M, Verny C, Dubas F, Procaccio V, Amati-Bonneau P, Bonneau D, Reynier P. 2009. Mitochondrial complex I deficiency in GDAP1-related autosomal dominant Charcot-Marie-Tooth disease (CMT2K). Neurogenetics 10:145-150.
13. Chevrollier A, Guillet V, Loiseau D, Gueguen N, de Crescenzo MA, Verny C, Ferre M, Dollfus H, Odent S, Milea D, Goizet C, Amati-Bonneau P, Procaccio V, Bonneau D, Reynier P. 2008. Hereditary optic neuropathies share a common mitochondrial coupling defect. Ann Neurol 63:794-798.
14. Coutinho P, Barros J, Zemmouri R, Guimaraes J, Alves C, Chorao R, Lourenco E, Ribeiro P, Loureiro JL, Santos JV, Hamri A, Paternotte C, Hazan J, Silva MC, Prud'homme JF, Grid D. 1999. Clinical heterogeneity of autosomal recessive spastic paraplegias: analysis of 106 patients in 46 families. Arch Neurol 56:943-949.
15. de Brito OM, Scorrano L. 2008. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605-610.
16. de Brito OM, Scorrano L. 2010. An intimate liaison: spatial organization of the endoplasmic reticulum-mitochondria relationship. Embo J 29:2715-2723.
17. Del Bo R, Moggio M, Rango M, Bonato S, D'Angelo MG, Ghezzi S, Airoldi G, Bassi MT, Guglieri M, Napoli L, Lamperti C, Corti S, Federico A, Bresolin N, Comi GP. 2008. Mutated mitofusin 2 presents with intrafamilial variability and brain mitochondrial dysfunction. Neurology 71:1959-1966.
18. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, Astarie-Dequeker C, Lasquellec L, Arnaud B, Ducommun B, Kaplan J, Hamel CP. 2000. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26:207-210.
19. Depienne C, Fedirko E, Forlani S, Cazeneuve C, Ribai P, Feki I, Tallaksen C, Nguyen K, Stankoff B, Ruberg M, Stevanin G, Durr A, Brice A. 2007a. Exon deletions of SPG4 are a frequent cause of hereditary spastic paraplegia. J Med Genet 44:281-284.
20. Depienne C, Tallaksen C, Lephay JY, Bricka B, Poea-Guyon S, Fontaine B, Labauge P, Brice A, Durr A. 2006. Spastin mutations are frequent in sporadic spastic paraparesis and their spectrum is different from that observed in familial cases. J Med Genet 43:259-265.
21. Depienne C, Stevanin G, Brice A, Durr A. 2007b. Hereditary spastic paraplegias: an update. Curr Opin Neurol 20:674-680.
22. Dubowitz V. 1985. Muscle biopsy: a practical approach, 2nd edition. London: Baillière Tindall.
23. Dubowitz V, Sewry CA. 2007. Muscle biopsy: a practical approach, 3rd edition. Saunders Elsevier.
24. Erichsen AK, Koht J, Stray-Pedersen A, Abdelnoor M, Tallaksen CM. 2009. Prevalence of hereditary ataxia and spastic paraplegia in southeast Norway: a population-based study. Brain 132:1577-1588.
25. Filla A, De Michele G, Marconi R, Bucci L, Carillo C, Castellano AE, Iorio L, Kniahynicki C, Rossi F, Campanella G. 1992. Prevalence of hereditary ataxias and spastic paraplegias in Molise, a region of Italy. J Neurol 239:351-353.
26. Fink JK. 2006. Hereditary spastic paraplegia. Curr Neurol Neurosci Rep 6:65-76.
27. Goizet C, Boukhris A, Durr A, Beetz C, Truchetto J, Tesson C, Tsaousidou M, Forlani S, Guyant-Marechal L, Fontaine B, Guimaraes J, Isidor B, Chazouilleres O, Wendum D, Grid D, Chevy F, Chinnery PF, Coutinho P, Azulay JP, Feki I, Mochel F, Wolf C, Mhiri C, Crosby A, Brice A, Stevanin G. 2009a. CYP7B1 mutations in pure and complex forms of hereditary spastic paraplegia type 5. Brain 132:1589-1600.
28. Goizet C, Boukhris A, Mundwiller E, Tallaksen C, Forlani S, Toutain A, Carriere N, Paquis V, Depienne C, Durr A, Stevanin G, Brice A. 2009b. Complicated forms of autosomal dominant hereditary spastic paraplegia are frequent in SPG10. Hum Mutat 30:E376-E385.
29. Harding AE. 1983. Classification of the hereditary ataxias and paraplegias. Lancet 1:1151-1155.
30. Hayashi T, Rizzuto R, Hajnoczky G, Su TP. 2009. MAM: more than just a housekeeper. Trends Cell Biol 19:81-88.
31. Hewamadduma C, McDermott C, Kirby J, Grierson A, Panayi M, Dalton A, Rajabally Y, Shaw P. 2009. New pedigrees and novel mutation expand the phenotype of REEP1-associated hereditary spastic paraplegia (HSP). Neurogenetics 10:105-110.
32. Ito D, Suzuki N. 2009. Seipinopathy: a novel endoplasmic reticulum stress-associated disease. Brain 132:8-15.
33. Klebe S, Lacour A, Durr A, Stojkovic T, Depienne C, Forlani S, Poea-Guyon S, Vuillaume I, Sablonniere B, Vermersch P, Brice A, Stevanin G. 2007. NIPA1 (SPG6) mutations are a rare cause of autosomal dominant spastic paraplegia in Europe. Neurogenetics 8:155-157.
34. Letellier T, Malgat M, Coquet M, Moretto B, Parrot-Roulaud F, Mazat JP. 1992. Mitochondrial myopathy studies on permeabilized muscle fibers. Pediatr Res 32:17-22.
35. Liu SG, Che FY, Heng XY, Li FF, Huang SZ, Lu de G, Hou SJ, Liu SE, Wang Q, Wang HP, Ma X. 2009. Clinical and genetic study of a novel mutation in the REEP1 gene. Synapse 63:201-205.
36. Loiseau D, Chevrollier A, Verny C, Guillet V, Gueguen N, Pou de Crescenzo MA, Ferre M, Malinge MC, Guichet A, Nicolas G, Amati-Bonneau P, Malthiery Y, Bonneau D, Reynier P. 2007. Mitochondrial coupling defect in Charcot-Marie-Tooth type 2A disease. Ann Neurol 61:315-323.
37. McDermott CJ, Taylor RW, Hayes C, Johnson M, Bushby KM, Turnbull DM, Shaw PJ. 2003. Investigation of mitochondrial function in hereditary spastic paraparesis. Neuroreport 14:485-488.
38. Merkwirth C, Langer T. 2008. Mitofusin 2 builds a bridge between ER and mitochondria. Cell 135:1165-1167.
39. Namekawa M, Ribai P, Nelson I, Forlani S, Fellmann F, Goizet C, Depienne C, Stevanin G, Ruberg M, Durr A, Brice A. 2006. SPG3A is the most frequent cause of hereditary spastic paraplegia with onset before age 10 years. Neurology 66:112-114.
40. Noensie EN, Dietz HC. 2001. A strategy for disease gene identification through nonsense-mediated mRNA decay inhibition. Nat Biotechnol 19:434-439.
41. Osman C, Voelker DR, Langer T. 2011. Making heads or tails of phospholipids in mitochondria. J Cell Biol 192:7-16.
42. Park SH, Zhu PP, Parker RL, Blackstone C. 2010. Hereditary spastic paraplegia proteins REEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. J Clin Invest 120:1097-1110.
43. Polo JM, Calleja J, Combarros O, Berciano J. 1993. Hereditary "pure" spastic paraplegia: a study of nine families. J Neurol Neurosurg Psychiatry 56:175-181.
44. Saito H, Kubota M, Roberts RW, Chi Q, Matsunami H. 2004. RTP family members induce functional expression of mammalian odorant receptors. Cell 119:679-691.
45. Salameh JS, Shenoy AM, David WS. 2009. Novel SPG3A and SPG4 mutations in two patients with Silver syndrome. J Clin Neuromuscul Dis 11:57-59.
46. Salinas S, Proukakis C, Crosby A, Warner TT. 2008. Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms. Lancet Neurol 7:1127-1138.
47. Schlang KJ, Arning L, Epplen JT, Stemmler S. 2008. Autosomal dominant hereditary spastic paraplegia: novel mutations in the REEP1 gene (SPG31). BMC Med Genet 9:71.
48. Schlipf NA, Beetz C, Schule R, Stevanin G, Erichsen AK, Forlani S, Zaros C, Karle K, Klebe S, Klimpe S, Durr A, Otto S, Tallaksen CM, Riess O, Brice A, Bauer P, Schols L. 2010. A total of 220 patients with autosomal dominant spastic paraplegia do not display mutations in the SLC33A1 gene (SPG42). Eur J Hum Genet 18:1065-1067.
49. Stevanin G, Ruberg M, Brice A. 2008. Recent advances in the genetics of spastic paraplegias. Curr Neurol Neurosci Rep 8:198-210.
50. Tzschach A, Graul-Neumann LM, Konrat K, Richter R, Ebert G, Ullmann R, Neitzel H. 2009. Interstitial deletion 2p11.2-p12: report of a patient with mental retardation and review of the literature. Am J Med Genet A 149A:242-245.
51. Waterham HR, Koster J, van Roermund CW, Mooyer PA, Wanders RJ, Leonard JV. 2007. A lethal defect of mitochondrial and peroxisomal fission. N Engl J Med 356:1736-1741.
52. Windpassinger C, Auer-Grumbach M, Irobi J, Patel H, Petek E, Horl G, Malli R, Reed JA, Dierick I, Verpoorten N, Warner TT, Proukakis C, Van den Bergh P, Verellen C, Van Maldergem L, Merlini L, De Jonghe P, Timmerman V, Crosby AH, Wagner K. 2004. Heterozygous missense mutations in BSCL2 are associated with distal hereditary motor neuropathy and Silver syndrome. Nat Genet 36:271-276.
53. Yu-Wai-Man P, Griffiths PG, Gorman GS, Lourenco CM, Wright AF, Auer-Grumbach M, Toscano A, Musumeci O, Valentino ML, Caporali L, Lamperti C, Tallaksen CM, Duffey P, Miller J, Whittaker RG, Baker MR, Jackson MJ, Clarke MP, Dhillon B, Czermin B, Stewart JD, Hudson G, Reynier P, Bonneau D, Marques W. Jr, Lenaers G, McFarland R, Taylor RW, Turnbull DM, Votruba M, Zeviani M, Carelli V, Bindoff LA, Horvath R, Amati-Bonneau P, Chinnery PF. 2010. Multi-system neurological disease is common in patients with OPA1 mutations. Brain 133:771-786.
54. Zuchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL, Zappia M, Nelis E, Patitucci A, Senderek J, Parman Y, Evgrafov O, Jonghe PD, Takahashi Y, Tsuji S, Pericak-Vance MA, Quattrone A, Battaloglu E, Polyakov AV, Timmerman V, Schroder JM, Vance JM. 2004. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 36:449-451.
55. Zuchner S, Wang G, Tran-Viet KN, Nance MA, Gaskell PC, Vance JM, Ashley-Koch AE, Pericak-Vance MA. 2006. Mutations in the novel mitochondrial protein REEP1 cause hereditary spastic paraplegia type 31. Am J Hum Genet 79:365-369.