Alteration of fatty-acid-metabolizing enzymes affects mitochondrial form and function in hereditary spastic paraplegia

American Journal of Human Genetics

Volumn 91, Issue 6, 2012, Pages 1051-1064

  Tesson, Christelle ^a,b,c,d   Nawara, Magdalena ^a,b,c   Salih, Mustafa A M ^e   Rossignol, Rodrigue ^f   Zaki, Maha S ^g   Al Balwi, Mohammed ^h,i   Schule, Rebecca ^j   Mignot, Cyril ^k   Obre, Emilie ^f   Bouhouche, Ahmed ^l   Santorelli, Filippo M ^m   Durand, Christelle M ^f   Oteyza, Andrés Caballero ^j   El Hachimi, Khalid H ^a,b,c,d   Al Drees, Abdulmajeed ^e   Bouslam, Naima ^l   Lamari, Foudil ^k   Elmalik, Salah A ^e   Kabiraj, Mohammad M ⁿ   Seidahmed, Mohammed Z ^o   Esteves, Typhaine ^a,b,c   Gaussen, Marion ^a,b,c   Monin, Marie Lorraine ^a,b,c   Gyapay, Gabor ^p   Lechner, Doris ^q   Gonzalez, Michael ^r   Depienne, Christel ^a,b,c,k   Mochel, Fanny ^a,b,c,k   Lavie, Julie ^f   Schols, Ludger ^j,s   Lacombe, Didier ^f,t   Yahyaoui, Mohamed ^l   Al Abdulkareem, Ibrahim ⁱ   Zuchner, Stephan ^r   Yamashita, Atsushi ^u   Benomar, Ali ^l   Goizet, Cyril ^f,t   Durr, Alexandra ^a,b,c,k   Gleeson, Joseph G ^v   Darios, Frederic ^a,b,c   Brice, Alexis ^a,b,c,k   Stevanin, Giovanni ^a,b,c,d,k   more..

^a INSERM   (France)

^b INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^c CNRS   (France)

^d PSL RESEARCH UNIVERSITY   (France)

^e KING SAUD UNIVERSITY   (Saudi Arabia)

^f Laboratoire Maladies Rares Génétique et Métabolisme Bordeaux University   (France)

^g NATIONAL RESEARCH CENTRE   (Egypt)

^h KING SAUD BIN ABDULAZIZ UNIVERSITY FOR HEALTH SCIENCES   (Saudi Arabia)

ⁱ KING SAUD BIN ABDULAZIZ UNIVERSITY FOR HEALTH SCIENCES   (Saudi Arabia)

^j UNIVERSITY OF TÜBINGEN   (Germany)

^k ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^l MOHAMMED V UNIVERSITY   (Morocco)

^m Istituto di Ricovero e Cura A Carattere Scientifico Fondazione Stella Maris   (Italy)

ⁿ The General Directorate of Armed Forces Health Services   (Saudi Arabia)

^o SECURITY FORCES HOSPITAL   (Saudi Arabia)

^p CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^q CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^r UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^s GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^t BORDEAUX UNIVERSITY HOSPITAL   (France)

^u TEIKYO UNIVERSITY   (Japan)

^v UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; DNA; MESSENGER RNA;

ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; ENZYME ACTIVITY; FATTY ACID METABOLISM; GENE MUTATION; GENETIC LINKAGE; HEREDITARY MOTOR SENSORY NEUROPATHY; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; LEG MUSCLE; MAJOR CLINICAL STUDY; MITOCHONDRION; NEXT GENERATION SEQUENCING; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SPASTICITY;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; CHROMOSOME MAPPING; CYTOCHROME P-450 ENZYME SYSTEM; FATTY ACIDS; FEMALE; GENE EXPRESSION PROFILING; GENOTYPE; HUMANS; INFANT; INFANT, NEWBORN; MALE; MITOCHONDRIA; MUTATION; PHENOTYPE; PHOSPHOLIPASES; PROTEIN TRANSPORT; SPASTIC PARAPLEGIA, HEREDITARY; YOUNG ADULT;

EID: 84870900912     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2012.11.001     Document Type: Article

References (65)

1. A.E. Harding Classification of the hereditary ataxias and paraplegias Lancet 1 1983 1151 1155 (Pubitemid 13084682)
2. C.M. Tallaksen, A. Dürr, and A. Brice Recent advances in hereditary spastic paraplegia Curr. Opin. Neurol. 14 2001 457 463 (Pubitemid 32703537)
3. J.K. Fink Advances in the hereditary spastic paraplegias Exp. Neurol. 184 Suppl 1 2003 S106 S110
4. R. Schüle, and L. Schöls Genetics of hereditary spastic paraplegias Semin. Neurol. 31 2011 484 493
5. J. Finsterer, W. Löscher, S. Quasthoff, J. Wanschitz, M. Auer-Grumbach, and G. Stevanin Hereditary spastic paraplegias with autosomal dominant, recessive, X-linked, or maternal trait of inheritance J. Neurol. Sci. 318 2012 1 18
6. S. Salinas, C. Proukakis, A. Crosby, and T.T. Warner Hereditary spastic paraplegia: Clinical features and pathogenetic mechanisms Lancet Neurol. 7 2008 1127 1138
7. G. Stevanin, M. Ruberg, and A. Brice Recent advances in the genetics of spastic paraplegias Curr. Neurol. Neurosci. Rep. 8 2008 198 210
8. C. Blackstone, C.J. O'Kane, and E. Reid Hereditary spastic paraplegias: Membrane traffic and the motor pathway Nat. Rev. Neurosci. 12 2011 31 42
9. P. Coutinho, J. Barros, R. Zemmouri, J. Guimarães, C. Alves, R. Chorão, E. Lourenço, P. Ribeiro, J.L. Loureiro, and J.V. Santos Clinical heterogeneity of autosomal recessive spastic paraplegias: Analysis of 106 patients in 46 families Arch. Neurol. 56 1999 943 949 (Pubitemid 29374811)
10. A. Boukhris, G. Stevanin, I. Feki, P. Denora, N. Elleuch, M.I. Miladi, C. Goizet, J. Truchetto, S. Belal, A. Brice, and C. Mhiri Tunisian hereditary spastic paraplegias: Clinical variability supported by genetic heterogeneity Clin. Genet. 75 2009 527 536
11. N. Bouslam, A. Benomar, H. Azzedine, A. Bouhouche, M. Namekawa, S. Klebe, C. Charon, A. Durr, M. Ruberg, and A. Brice Mapping of a new form of pure autosomal recessive spastic paraplegia (SPG28) Ann. Neurol. 57 2005 567 571 (Pubitemid 40471170)
12. G. Casari, M. De Fusco, S. Ciarmatori, M. Zeviani, M. Mora, P. Fernandez, G. De Michele, A. Filla, S. Cocozza, and R. Marconi Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease Cell 93 1998 973 983 (Pubitemid 28280791)
13. C. Goizet, A. Boukhris, A. Durr, C. Beetz, J. Truchetto, C. Tesson, M. Tsaousidou, S. Forlani, L. Guyant-Maréchal, and B. Fontaine CYP7B1 mutations in pure and complex forms of hereditary spastic paraplegia type 5 Brain 132 2009 1589 1600
14. S. Klebe, A. Lossos, H. Azzedine, E. Mundwiller, R. Sheffer, M. Gaussen, C. Marelli, M. Nawara, W. Carpentier, and V. Meyer KIF1A missense mutations in SPG30, an autosomal recessive spastic paraplegia: Distinct phenotypes according to the nature of the mutations Eur. J. Hum. Genet. 20 2012 645 649
15. M.K. Tsaousidou, K. Ouahchi, T.T. Warner, Y. Yang, M.A. Simpson, N.G. Laing, P.A. Wilkinson, R.E. Madrid, H. Patel, and F. Hentati Sequence alterations within CYP7B1 implicate defective cholesterol homeostasis in motor-neuron degeneration Am. J. Hum. Genet. 82 2008 510 515
16. G. Stevanin, H. Azzedine, P. Denora, A. Boukhris, M. Tazir, A. Lossos, A.L. Rosa, I. Lerer, A. Hamri, P. Alegria SPATAX consortium Mutations in SPG11 are frequent in autosomal recessive spastic paraplegia with thin corpus callosum, cognitive decline and lower motor neuron degeneration Brain 131 2008 772 784 (Pubitemid 351294708)
17. G.R. Abecasis, S.S. Cherny, W.O. Cookson, and L.R. Cardon Merlin - Rapid analysis of dense genetic maps using sparse gene flow trees Nat. Genet. 30 2002 97 101
18. I.A. Adzhubei, S. Schmidt, L. Peshkin, V.E. Ramensky, A. Gerasimova, P. Bork, A.S. Kondrashov, and S.R. Sunyaev A method and server for predicting damaging missense mutations Nat. Methods 7 2010 248 249
19. J.M. Schwarz, C. Rödelsperger, M. Schuelke, and D. Seelow MutationTaster evaluates disease-causing potential of sequence alterations Nat. Methods 7 2010 575 576
20. R.P. Murmu, E. Martin, A. Rastetter, T. Esteves, M.-P. Muriel, K.H. El Hachimi, P.S. Denora, A. Dauphin, J.C. Fernandez, and C. Duyckaerts Cellular distribution and subcellular localization of spatacsin and spastizin, two proteins involved in hereditary spastic paraplegia Mol. Cell. Neurosci. 47 2011 191 202
21. C. Jose, E. Hébert-Chatelain, N. Bellance, A. Larendra, M. Su, K. Nouette-Gaulain, and R. Rossignol AICAR inhibits cancer cell growth and triggers cell-type distinct effects on OXPHOS biogenesis, oxidative stress and Akt activation Biochim. Biophys. Acta 1807 2011 707 718
22. G. Benard, B. Faustin, E. Passerieux, A. Galinier, C. Rocher, N. Bellance, J.-P. Delage, L. Casteilla, T. Letellier, and R. Rossignol Physiological diversity of mitochondrial oxidative phosphorylation Am. J. Physiol. Cell Physiol. 291 2006 C1172 C1182
23. G. Benard, N. Bellance, D. James, P. Parrone, H. Fernandez, T. Letellier, and R. Rossignol Mitochondrial bioenergetics and structural network organization J. Cell Sci. 120 2007 838 848 (Pubitemid 46523485)
24. Q. Li, A. Lau, T.J. Morris, L. Guo, C.B. Fordyce, and E.F. Stanley A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization J. Neurosci. 24 2004 4070 4081 (Pubitemid 38544233)
25. M. Brown, D. Adyshev, V. Bindokas, J. Moitra, J.G.N. Garcia, and S.M. Dudek Quantitative distribution and colocalization of non-muscle myosin light chain kinase isoforms and cortactin in human lung endothelium Microvasc. Res. 80 2010 75 88
26. F. Darios, N. Lambeng, J.-D. Troadec, P.P. Michel, and M. Ruberg Ceramide increases mitochondrial free calcium levels via caspase 8 and Bid: role in initiation of cell death J. Neurochem. 84 2003 643 654 (Pubitemid 36176923)
27. H.N. Higgs, M.H. Han, G.E. Johnson, and J.A. Glomset Cloning of a phosphatidic acid-preferring phospholipase A1 from bovine testis J. Biol. Chem. 273 1998 5468 5477 (Pubitemid 28124010)
28. S.S. Chuang, C. Helvig, M. Taimi, H.A. Ramshaw, A.H. Collop, M. Amad, J.A. White, M. Petkovich, G. Jones, and B. Korczak CYP2U1, a novel human thymus- and brain-specific cytochrome P450, catalyzes omega- and (omega-1)- hydroxylation of fatty acids J. Biol. Chem. 279 2004 6305 6314 (Pubitemid 38248763)
29. M. Karlgren, M. Backlund, I. Johansson, M. Oscarson, and M. Ingelman-Sundberg Characterization and tissue distribution of a novel human cytochrome P450-CYP2U1 Biochem. Biophys. Res. Commun. 315 2004 679 685 (Pubitemid 38229397)
30. A. Yamashita, T. Kumazawa, H. Koga, N. Suzuki, S. Oka, and T. Sugiura Generation of lysophosphatidylinositol by DDHD domain containing 1 (DDHD1): Possible involvement of phospholipase D/phosphatidic acid in the activation of DDHD1 Biochim. Biophys. Acta 1801 2010 711 720
31. F. Dutheil, S. Dauchy, M. Diry, V. Sazdovitch, O. Cloarec, L. Mellottée, I. Bièche, M. Ingelman-Sundberg, J.-P. Flinois, and I. de Waziers Xenobiotic-metabolizing enzymes and transporters in the normal human brain: Regional and cellular mapping as a basis for putative roles in cerebral function Drug Metab. Dispos. 37 2009 1528 1538
32. E.I. Rugarli, and T. Langer Mitochondrial quality control: A matter of life and death for neurons EMBO J. 31 2012 1336 1349
33. G. Benard, and R. Rossignol Mitochondrial fluidity matters. Focus on "Inherited complex I deficiency is associated with faster protein diffusion in the matrix of moving mitochondria" Am. J. Physiol. Cell Physiol. 294 2008 C1123
34. S. Hanein, E. Martin, A. Boukhris, P. Byrne, C. Goizet, A. Hamri, A. Benomar, A. Lossos, P. Denora, and J. Fernandez Identification of the SPG15 gene, encoding spastizin, as a frequent cause of complicated autosomal-recessive spastic paraplegia, including Kjellin syndrome Am. J. Hum. Genet. 82 2008 992 1002
35. G. Stevanin, F.M. Santorelli, H. Azzedine, P. Coutinho, J. Chomilier, P.S. Denora, E. Martin, A.-M. Ouvrard-Hernandez, A. Tessa, and N. Bouslam Mutations in SPG11, encoding spatacsin, are a major cause of spastic paraplegia with thin corpus callosum Nat. Genet. 39 2007 366 372 (Pubitemid 46328495)
36. H.N. Higgs, and J.A. Glomset Identification of a phosphatidic acid-preferring phospholipase A1 from bovine brain and testis Proc. Natl. Acad. Sci. USA 91 1994 9574 9578 (Pubitemid 24297957)
37. K. Tani, T. Mizoguchi, A. Iwamatsu, K. Hatsuzawa, and M. Tagaya p125 is a novel mammalian Sec23p-interacting protein with structural similarity to phospholipid-modifying proteins J. Biol. Chem. 274 1999 20505 20512
38. K. Nakajima, H. Sonoda, T. Mizoguchi, J. Aoki, H. Arai, M. Nagahama, M. Tagaya, and K. Tani A novel phospholipase A1 with sequence homology to a mammalian Sec23p-interacting protein, p125 J. Biol. Chem. 277 2002 11329 11335 (Pubitemid 34952898)
39. D. Gebremedhin, A.R. Lange, J. Narayanan, M.R. Aebly, E.R. Jacobs, and D.R. Harder Cat cerebral arterial smooth muscle cells express cytochrome P450 4A2 enzyme and produce the vasoconstrictor 20-HETE which enhances L-type Ca2+ current J. Physiol. 507 1998 771 781 (Pubitemid 28143578)
40. M.A. Carroll, and J.C. McGiff A new class of lipid mediators: Cytochrome P450 arachidonate metabolites Thorax 55 Suppl 2 2000 S13 S16
41. J.D. Imig, B.T. Pham, E.A. LeBlanc, K.M. Reddy, J.R. Falck, and E.W. Inscho Cytochrome P450 and cyclooxygenase metabolites contribute to the endothelin-1 afferent arteriolar vasoconstrictor and calcium responses Hypertension 35 2000 307 312 (Pubitemid 30054191)
42. P.-A. Chang, and Y.-J. Wu Neuropathy target esterase: An essential enzyme for neural development and axonal maintenance Int. J. Biochem. Cell Biol. 42 2010 573 575
43. M.A. Aldahmesh, J.Y. Mohamed, H.S. Alkuraya, I.C. Verma, R.D. Puri, A.A. Alaiya, W.B. Rizzo, and F.S. Alkuraya Recessive mutations in ELOVL4 cause ichthyosis, intellectual disability, and spastic quadriplegia Am. J. Hum. Genet. 89 2011 745 750
44. A. Gregory, and S.J. Hayflick Genetics of neurodegeneration with brain iron accumulation Curr. Neurol. Neurosci. Rep. 11 2011 254 261
45. R.H. Schaloske, and E.A. Dennis The phospholipase A2 superfamily and its group numbering system Biochim. Biophys. Acta 1761 2006 1246 1259 (Pubitemid 44755364)
46. P.C. Kienesberger, M. Oberer, A. Lass, and R. Zechner Mammalian patatin domain containing proteins: A family with diverse lipolytic activities involved in multiple biological functions J. Lipid Res. 50 Suppl 2009 S63 S68
47. S. Oka, K. Nakajima, A. Yamashita, S. Kishimoto, and T. Sugiura Identification of GPR55 as a lysophosphatidylinositol receptor Biochem. Biophys. Res. Commun. 362 2007 928 934 (Pubitemid 47390663)
48. S. Oka, T. Toshida, K. Maruyama, K. Nakajima, A. Yamashita, and T. Sugiura 2-Arachidonoyl-sn-glycero-3-phosphoinositol: A possible natural ligand for GPR55 J. Biochem. 145 2009 13 20
49. S. Oka, R. Ota, M. Shima, A. Yamashita, and T. Sugiura GPR35 is a novel lysophosphatidic acid receptor Biochem. Biophys. Res. Commun. 395 2010 232 237
50. S. Anavi-Goffer, G. Baillie, A.J. Irving, J. Gertsch, I.R. Greig, R.G. Pertwee, and R.A. Ross Modulation of L-α-lysophosphatidylinositol/GPR55 mitogen-activated protein kinase (MAPK) signaling by cannabinoids J. Biol. Chem. 287 2012 91 104
51. N. Rimmerman, H.B. Bradshaw, A. Basnet, B. Tan, T.S. Widlanski, and J.M. Walker Microsomal omega-hydroxylated metabolites of N-arachidonoyl dopamine are active at recombinant human TRPV1 receptors Prostaglandins Other Lipid Mediat. 88 2009 10 17
52. H. Wen, J. Östman, K.J. Bubb, C. Panayiotou, J.V. Priestley, M.D. Baker, and A. Ahluwalia 20-Hydroxyeicosatetraenoic acid (20-HETE) is a novel activator of transient receptor potential vanilloid 1 (TRPV1) channel J. Biol. Chem. 287 2012 13868 13876
53. 1 receptors regulate neuronal energy metabolism Nat. Neurosci. 15 2012 558 564
54. R. Steenbergen, T.S. Nanowski, A. Beigneux, A. Kulinski, S.G. Young, and J.E. Vance Disruption of the phosphatidylserine decarboxylase gene in mice causes embryonic lethality and mitochondrial defects J. Biol. Chem. 280 2005 40032 40040 (Pubitemid 41779137)
55. K. Brandner, D.U. Mick, A.E. Frazier, R.D. Taylor, C. Meisinger, and P. Rehling Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth Syndrome Mol. Biol. Cell 16 2005 5202 5214 (Pubitemid 41566832)
56. S.-Y. Choi, P. Huang, G.M. Jenkins, D.C. Chan, J. Schiller, and M.A. Frohman A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis Nat. Cell Biol. 8 2006 1255 1262 (Pubitemid 44660590)
57. G. Benard, and M. Karbowski Mitochondrial fusion and division: Regulation and role in cell viability Semin. Cell Dev. Biol. 20 2009 365 374
58. A. Niemann, K.M. Wagner, M. Ruegg, and U. Suter GDAP1 mutations differ in their effects on mitochondrial dynamics and apoptosis depending on the mode of inheritance Neurobiol. Dis. 36 2009 509 520
59. C.-R. Chang, C.M. Manlandro, D. Arnoult, J. Stadler, A.E. Posey, R.B. Hill, and C. Blackstone A lethal de novo mutation in the middle domain of the dynamin-related GTPase Drp1 impairs higher order assembly and mitochondrial division J. Biol. Chem. 285 2010 32494 32503
60. C. Goizet, C. Depienne, G. Benard, A. Boukhris, E. Mundwiller, G. Solé, I. Coupry, J. Pilliod, M.-L. Martin-Négrier, and E. Fedirko REEP1 mutations in SPG31: frequency, mutational spectrum, and potential association with mitochondrial morpho-functional dysfunction Hum. Mutat. 32 2011 1118 1127
61. A. Chevrollier, J. Cassereau, M. Ferré, J. Alban, V. Desquiret-Dumas, N. Gueguen, P. Amati-Bonneau, V. Procaccio, D. Bonneau, and P. Reynier Standardized mitochondrial analysis gives new insights into mitochondrial dynamics and OPA1 function Int. J. Biochem. Cell Biol. 44 2012 980 988
62. M. Girard, R. Larivière, D.A. Parfitt, E.C. Deane, R. Gaudet, N. Nossova, F. Blondeau, G. Prenosil, E.G.M. Vermeulen, and M.R. Duchen Mitochondrial dysfunction and Purkinje cell loss in autosomal recessive spastic ataxia of Charlevoix-Saguenay (ARSACS) Proc. Natl. Acad. Sci. USA 109 2012 1661 1666
63. A.L. Misko, Y. Sasaki, E. Tuck, J. Milbrandt, and R.H. Baloh Mitofusin2 mutations disrupt axonal mitochondrial positioning and promote axon degeneration J. Neurosci. 32 2012 4145 4155
64. K. Gücüyener, F.G. Pinarli, D. Erbaş, A. Hasanoǧlu, A. Serdaroǧlu, and H. Topaloǧlu Is oxidative damage in operation in patients with hereditary spastic paraparesis? Brain Dev. 32 2010 130 136
65. R. Schüle, T. Siddique, H.-X. Deng, Y. Yang, S. Donkervoort, M. Hansson, R.E. Madrid, N. Siddique, L. Schöls, and I. Björkhem Marked accumulation of 27-hydroxycholesterol in SPG5 patients with hereditary spastic paresis J. Lipid Res. 51 2010 819 823