Responsiveness of sphingosine phosphate lyase insufficiency syndrome to vitamin B6 cofactor supplementation
dc.contributor.author | Zhao, Piming | |
dc.contributor.author | Liu, Isaac D. | |
dc.contributor.author | Hodgin, Jeffrey B. | |
dc.contributor.author | Benke, Peter I. | |
dc.contributor.author | Selva, Jeremy | |
dc.contributor.author | Torta, Federico | |
dc.contributor.author | Wenk, Markus R. | |
dc.contributor.author | Endrizzi, James A. | |
dc.contributor.author | West, Olivia | |
dc.contributor.author | Ou, Weixing | |
dc.contributor.author | Tang, Emily | |
dc.contributor.author | Goh, Denise Li‐meng | |
dc.contributor.author | Tay, Stacey Kiat‐hong | |
dc.contributor.author | Yap, Hui‐kim | |
dc.contributor.author | Loh, Alwin | |
dc.contributor.author | Weaver, Nicole | |
dc.contributor.author | Sullivan, Bonnie | |
dc.contributor.author | Larson, Austin | |
dc.contributor.author | Cooper, Megan A. | |
dc.contributor.author | Alhasan, Khalid | |
dc.contributor.author | Alangari, Abdullah A. | |
dc.contributor.author | Salim, Suha | |
dc.contributor.author | Gumus, Evren | |
dc.contributor.author | Chen, Karin | |
dc.contributor.author | Zenker, Martin | |
dc.contributor.author | Hildebrandt, Friedhelm | |
dc.contributor.author | Saba, Julie D. | |
dc.date.accessioned | 2020-10-01T23:29:31Z | |
dc.date.available | WITHHELD_12_MONTHS | |
dc.date.available | 2020-10-01T23:29:31Z | |
dc.date.issued | 2020-09 | |
dc.identifier.citation | Zhao, Piming; Liu, Isaac D.; Hodgin, Jeffrey B.; Benke, Peter I.; Selva, Jeremy; Torta, Federico; Wenk, Markus R.; Endrizzi, James A.; West, Olivia; Ou, Weixing; Tang, Emily; Goh, Denise Li‐meng ; Tay, Stacey Kiat‐hong ; Yap, Hui‐kim ; Loh, Alwin; Weaver, Nicole; Sullivan, Bonnie; Larson, Austin; Cooper, Megan A.; Alhasan, Khalid; Alangari, Abdullah A.; Salim, Suha; Gumus, Evren; Chen, Karin; Zenker, Martin; Hildebrandt, Friedhelm; Saba, Julie D. (2020). "Responsiveness of sphingosine phosphate lyase insufficiency syndrome to vitamin B6 cofactor supplementation." Journal of Inherited Metabolic Disease 43(5): 1131-1142. | |
dc.identifier.issn | 0141-8955 | |
dc.identifier.issn | 1573-2665 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/162713 | |
dc.description.abstract | Sphingosine- 1- phosphate (S1P) lyase is a vitamin B6- dependent enzyme that degrades sphingosine- 1- phosphate in the final step of sphingolipid metabolism. In 2017, a new inherited disorder was described caused by mutations in SGPL1, which encodes sphingosine phosphate lyase (SPL). This condition is referred to as SPL insufficiency syndrome (SPLIS) or alternatively as nephrotic syndrome type 14 (NPHS14). Patients with SPLIS exhibit lymphopenia, nephrosis, adrenal insufficiency, and/or neurological defects. No targeted therapy for SPLIS has been reported. Vitamin B6 supplementation has therapeutic activity in some genetic diseases involving B6- dependent enzymes, a finding ascribed largely to the vitamin’s chaperone function. We investigated whether B6 supplementation might have activity in SPLIS patients. We retrospectively monitored responses of disease biomarkers in patients supplemented with B6 and measured SPL activity and sphingolipids in B6- treated patient- derived fibroblasts. In two patients, disease biomarkers responded to B6 supplementation. S1P abundance and activity levels increased and sphingolipids decreased in response to B6. One responsive patient is homozygous for an SPL R222Q variant present in almost 30% of SPLIS patients. Molecular modeling suggests the variant distorts the dimer interface which could be overcome by cofactor supplementation. We demonstrate the first potential targeted therapy for SPLIS and suggest that 30% of SPLIS patients might respond to cofactor supplementation. | |
dc.publisher | John Wiley & Sons, Inc. | |
dc.subject.other | sphingosine- 1- phosphate | |
dc.subject.other | pyridoxal 5- ²- phosphate | |
dc.subject.other | SGPL1 | |
dc.subject.other | sphingolipidosis | |
dc.subject.other | sphingosine phosphate lyase | |
dc.subject.other | SPL insufficiency syndrome | |
dc.subject.other | vitamin B6 | |
dc.title | Responsiveness of sphingosine phosphate lyase insufficiency syndrome to vitamin B6 cofactor supplementation | |
dc.type | Article | |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Medicine (General) | |
dc.subject.hlbtoplevel | Health Sciences | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/162713/2/jimd12238.pdf | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/162713/1/jimd12238_am.pdf | en_US |
dc.identifier.doi | 10.1002/jimd.12238 | |
dc.identifier.source | Journal of Inherited Metabolic Disease | |
dc.identifier.citedreference | Yu FPS, Amintas S, Levade T, Medin JA. Acid ceramidase deficiency: Farber disease and SMA- PME. Orphanet J Rare Dis. 2018; 13: 121. | |
dc.identifier.citedreference | Saba JD. Fifty years of lyase and a moment of truth: sphingosine phosphate lyase from discovery to disease. J Lipid Res. 2019; 60: 456 - 463. | |
dc.identifier.citedreference | Van Veldhoven PP. Sphingosine- 1- phosphate lyase. Methods Enzymol. 2000; 311: 244 - 254. | |
dc.identifier.citedreference | Atkinson D, Nikodinovic Glumac J, Asselbergh B, et al. Sphingosine 1- phosphate lyase deficiency causes Charcot- Marie- tooth neuropathy. Neurology. 2017; 88: 533 - 542. | |
dc.identifier.citedreference | Janecke AR, Xu R, Steichen- Gersdorf E, et al. Deficiency of the sphingosine- 1- phosphate lyase SGPL1 is associated with congenital nephrotic syndrome and congenital adrenal calcifications. Hum Mutat. 2017; 38: 365 - 372. | |
dc.identifier.citedreference | Linhares ND, Arantes RR, Araujo SA, Pena SDJ. Nephrotic syndrome and adrenal insufficiency caused by a variant in SGPL1. Clin Kidney J. 2018; 11:462- 467. | |
dc.identifier.citedreference | Lovric S, Goncalves S, Gee HY, et al. Mutations in sphingosine- 1- phosphate lyase cause nephrosis with ichthyosis and adrenal insufficiency. J Clin Invest. 2017; 127: 912 - 928. | |
dc.identifier.citedreference | Prasad R, Hadjidemetriou I, Maharaj A, et al. Sphingosine- 1- phosphate lyase mutations cause primary adrenal insufficiency and steroid- resistant nephrotic syndrome. J Clin Invest. 2017; 127: 942 - 953. | |
dc.identifier.citedreference | Cellini B, Montioli R, Oppici E, Astegno A, Voltattorni CB. The chaperone role of the pyridoxal 5- ²- phosphate and its implications for rare diseases involving B6- dependent enzymes. Clin Biochem. 2014; 47: 158 - 165. | |
dc.identifier.citedreference | Settas N, Persky R, Faucz FR, et al. SGPL1 deficiency: a rare cause of primary adrenal insufficiency. J Clin Endocrinol Metab. 2019; 104: 1484 - 1490. | |
dc.identifier.citedreference | Saygili S, Canpolat N, Sever L, Caliskan S, Atayar E, Ozaltin F. Persistent hypoglycemic attacks during hemodialysis sessions in an infant with congenital nephrotic syndrome: answers. Pediatr Nephrol. 2019; 34: 77 - 79. | |
dc.identifier.citedreference | Bamborschke D, Pergande M, Becker K, et al. A novel mutation in sphingosine- 1- phosphate lyase causing congenital brain malformation. Brain Dev. 2018; 40: 480 - 483. | |
dc.identifier.citedreference | Choi YJ, Saba JD. Sphingosine phosphate lyase insufficiency syndrome (SPLIS): a novel inborn error of sphingolipid metabolism. Adv Biol Regul. 2019; 71: 128 - 140. | |
dc.identifier.citedreference | Arenz C. Recent advances and novel treatments for sphingolipidoses. Future Med Chem. 2017; 9: 1687 - 1700. | |
dc.identifier.citedreference | Hannun Y. Bioactive Sphingolipids in Cancer Biology and Therapy. Cham, Switzerland: Springer International; 2015. | |
dc.identifier.citedreference | Edvardson S, Yi JK, Jalas C, et al. Deficiency of the alkaline ceramidase ACER3 manifests in early childhood by progressive leukodystrophy. J Med Genet. 2016; 53: 389 - 396. | |
dc.identifier.citedreference | Dunn TM, Tifft CJ, Proia RL. A perilous path: the inborn errors of sphingolipid metabolism. J Lipid Res. 2019; 60: 475 - 483. | |
dc.identifier.citedreference | Gombart AF, Pierre A, Maggini S. A review of micronutrients and the immune system- working in harmony to reduce the risk of infection. Nutrients. 2020; 12: 236. | |
dc.identifier.citedreference | Vogel P, Donoviel MS, Read R, et al. Incomplete inhibition of sphingosine 1- phosphate lyase modulates immune system function yet prevents early lethality and non- lymphoid lesions. PLoS One. 2009; 4: e4112. | |
dc.identifier.citedreference | Lorenz EC, Lieske JC, Seide BM, et al. Sustained pyridoxine response in primary hyperoxaluria type 1 recipients of kidney alone transplant. Am J Transplant. 2014; 14: 1433 - 1438. | |
dc.identifier.citedreference | Hu FL, Gu Z, Kozich V, Kraus JP, Ramesh V, Shih VE. Molecular basis of cystathionine beta- synthase deficiency in pyridoxine responsive and nonresponsive homocystinuria. Hum Mol Genet. 1993; 2: 1857 - 1860. | |
dc.identifier.citedreference | Phillips RS. Chemistry and diversity of pyridoxal- 5- ²- phosphate dependent enzymes. Biochim Biophys Acta. 2015; 1854: 1167 - 1174. | |
dc.identifier.citedreference | Davis D, Kannan M, Wattenberg B. Orm/ORMDL proteins: gate guardians and master regulators. Adv Biol Regul. 2018; 70: 3 - 18. | |
dc.identifier.citedreference | Caro JA, Harpole KW, Kasinath V, et al. Entropy in molecular recognition by proteins. Proc Natl Acad Sci U S A. 2017; 114: 6563 - 6568. | |
dc.identifier.citedreference | Weiler S, Braendlin N, Beerli C, Bergsdorf C, Schubart A, Srinivas H, Oberhauser B, Billich A. Orally active 7- substituted(4- benzylphthalazin- 1- yl)- 2- methylpiperazin- 1- yl]nicotinonitriles asactive- site inhibitors of sphingosine 1- phosphate lyase for the treatment of multiple sclerosis. J Med Chem 2014; 57: 5074 - 5084. | |
dc.identifier.citedreference | Oppici E, Fargue S, Reid ES, et al. Pyridoxamine and pyridoxal are more effective than pyridoxine in rescuing folding- defective variants of human alanine:glyoxylate aminotransferase causing primary hyperoxaluria type I. Hum Mol Genet. 2015; 24: 5500 - 5511. | |
dc.identifier.citedreference | Thakar MS, Hintermeyer MK, Gries MG, Routes JM, Verbsky JW. A practical approach to newborn screening for severe combined immunodeficiency using the T cell receptor excision circle assay. Front Immunol. 2017; 8: 1470. | |
dc.identifier.citedreference | Schwab SR, Periera JP, Matloubian M, Xu Y, Huang Y, Cyster JG. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1Pgradients. Science. 2005; 309: 1735 - 1739. | |
dc.identifier.citedreference | Matloubian M, Lo CG, Cinamon G, et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 2004; 427: 355 - 360. | |
dc.identifier.citedreference | Morales E, Alonso M, Gutiérrez E. Collapsing glomerulopathy: update. Med Clin (Barc). 2019; 152: 361 - 367. | |
dc.identifier.citedreference | Reiss U, Oskouian B, Zhou J, et al. Sphingosine- phosphate lyase enhances stress- induced ceramide generation and apoptosis. J Biol Chem. 2004; 279: 1281 - 1290. | |
dc.identifier.citedreference | Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010; 66: 486 - 501. | |
dc.identifier.citedreference | Oskouian B, Sooriyakumaran P, Borowsky AD, et al. Sphingosine- 1- phosphate lyase potentiates apoptosis via p53- and p38- dependent pathways and is downregulated in colon cancer. Proc Natl Acad Sci U S A. 2006; 103: 17384 - 17389. | |
dc.identifier.citedreference | Suh JH, Degagné E, Gleghorn EE, et al. Sphingosine- 1- phosphate signaling and metabolism gene signature in pediatric inflammatory bowel disease: A matched- case control pilot study. Inflamm Bowel Dis. 2018; 24: 1321 - 1334. | |
dc.identifier.citedreference | Narayanaswamy P, Shinde S, Sulc R, et al. Lipidomic "deep profiling": an enhanced workflow to reveal new molecular species of signaling lipids. Anal Chem. 2014; 86: 3043 - 3047. | |
dc.identifier.citedreference | Suh JH, Eltanawy A, Rangan A, Saba JD. A facile stable- isotope dilution method for determination of sphingosine phosphate lyase activity. Chem Phys Lipids. 2016; 194: 101 - 109. | |
dc.identifier.citedreference | Vangipuram M, Ting D, Kim S, Diaz R, Schule B. Skin punch biopsy explant culture for derivation of primary human fibroblasts. J Vis Exp. 2013;July 7: e3779. | |
dc.identifier.citedreference | Clayton PT. B6- responsive disorders: a model of vitamin dependency. J Inherit Metab Dis. 2006; 29: 317 - 326. | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.