Publications

Lettieri A, Oleari R, van den Munkhof MH, van Battum EY, Verhagen MG, Tacconi C, Spreafico M, Paganoni AJJ, Azzarelli R, Andre’ V, Amoruso F, Palazzolo L, Eberini I, Dunkel L, Howard SR, Fantin A, Pasterkamp RJ, Cariboni A. SEMA6A drives GnRH neuron-dependent puberty onset by tuning median eminence vascular permeability. Nat Commun. 2023 Dec 7;14(1):8097. doi: 10.1038/s41467-023-43820-z.

Oleari, R., Lettieri, A., Manzini, S., Paganoni, A., André, V., Grazioli, P., Busnelli, M., Duminuco, P., Vitobello, A., Philippe, C., Bizaoui, V., Storr, H. L., Amoruso, F., Memi, F., Vezzoli, V., Massa, V., Scheiffele, P., Howard, S. R., & Cariboni, A. Combined omic analyses reveal autism-linked NLGN3 gene as a key developmental regulator of GnRH neuron biology and diseaseDisease models & mechanisms, 2023. dmm.049996. doi:10.1242/dmm.049996.

Paganoni AJJ, Amoruso F, Porta Pelayo J, Calleja-Pérez B, Vezzoli V, Duminuco P, Caramello A, Oleari R, Fernández-Jaén A, Cariboni A. A Novel Loss-of-Function SEMA3E Mutation in a Patient with Severe Intellectual Disability and Cognitive Regression. Int J Mol Sci. 2022 May 18;23(10):5632. doi: 10.3390/ijms23105632. PMID: 35628442; PMCID: PMC9143429.

Camera M, Russo I, Zamboni V, Ammoni A, Rando S, Morellato A, Cimino I, Angelini C, Giacobini P, Oleari R, Amoruso F, Cariboni A, Franceschini I, Turco E, Defilippi P, Merlo GR. p140Cap Controls Female Fertility in Mice Acting via Glutamatergic Afference on Hypothalamic Gonadotropin-Releasing Hormone Neurons. Front Neurosci. 2022 Feb 14;16:744693. doi: 10.3389/fnins.2022.744693. PMID: 35237119; PMCID: PMC8884249.

Whittaker DE, Oleari R, Gregory LC, Le Quesne-Stabej P, Williams HJ; GOSgene, Torpiano JG, Formosa N, Cachia MJ, Field D, Lettieri A, Ocaka LA, Paganoni AJ, Rajabali SH, Riegman KL, De Martini LB, Chaya T, Robinson IC, Furukawa T, Cariboni A, Basson MA, Dattani MT. A recessive PRDM13 mutation results in congenital hypogonadotropic hypogonadism and cerebellar hypoplasia. J Clin Invest. 2021 Dec 15;131(24):e141587. doi: 10.1172/JCI141587. PMID: 34730112; PMCID: PMC8670848.

Oleari R, Massa V, Cariboni A, Lettieri A. The Differential Roles for Neurodevelopmental and Neuroendocrine Genes in Shaping GnRH Neuron Physiology and Deficiency. Int J Mol Sci. 2021 Aug 30;22(17):9425. doi: 10.3390/ijms22179425. PMID: 34502334; PMCID: PMC8431607.

Lettieri A, Oleari R, Paganoni AJJ, Gervasini C, Massa V, Fantin A, Cariboni A. Semaphorin Regulation by the Chromatin Remodeler CHD7: An Emerging Genetic Interaction Shaping Neural Cells and Neural Crest in Development and Cancer. Front Cell Dev Biol. 2021 Apr 1;9:638674. doi: 10.3389/fcell.2021.638674. PMID: 33869187; PMCID: PMC8047133.

Cannarella R, Paganoni AJJ, Cicolari S, Oleari R, Condorelli RA, La Vignera S, Cariboni A, Calogero AE, Magni P. Anti-Müllerian Hormone, Growth Hormone, and Insulin-Like Growth Factor 1 Modulate the Migratory and Secretory Patterns of GnRH Neurons. Int J Mol Sci. 2021 Feb 28;22(5):2445. doi: 10.3390/ijms22052445. PMID: 33671044; PMCID: PMC7957759.

Cariboni A, Balasubramanian R. Kallmann syndrome and idiopathic hypogonadotropic hypogonadism: The role of semaphorin signaling on GnRH neurons. Handb Clin Neurol. 2021;182:307-315. doi: 10.1016/B978-0-12-819973-2.00022-8. PMID: 34266601; PMCID: PMC9039773.

Oleari R, André V, Lettieri A, Tahir S, Roth L, Paganoni A, Eberini I, Parravicini C, Scagliotti V, Cotellessa L, Bedogni F, De Martini LB, Corridori MV, Gulli S, Augustin HG, Gaston-Massuet C, Hussain K, Cariboni A. A Novel SEMA3G Mutation in Two Siblings Affected by Syndromic GnRH Deficiency. Neuroendocrinology. 2021;111(5):421-441. doi: 10.1159/000508375. Epub 2020 May 4. PMID: 32365351.

Mancini A, Howard SR, Marelli F, Cabrera CP, Barnes MR, Sternberg MJ, Leprovots M, Hadjidemetriou I, Monti E, David A, Wehkalampi K, Oleari R, Lettieri A, Vezzoli V, Vassart G, Cariboni A, Bonomi M, Garcia MI, Guasti L, Dunkel L. LGR4 deficiency results in delayed puberty through impaired Wnt/β-catenin signaling. JCI Insight. 2020 Jun 4;5(11):e133434. doi: 10.1172/jci.insight.133434. PMID: 32493844; PMCID: PMC7308048.

Lettieri A, Borgo C, Zanieri L, D’Amore C, Oleari R, Paganoni A, Pinna LA, Cariboni A, Salvi M. Protein Kinase CK2 Subunits Differentially Perturb the Adhesion and Migration of GN11 Cells: A Model of Immature Migrating Neurons. Int J Mol Sci. 2019 Nov 26;20(23):5951. doi: 10.3390/ijms20235951. PMID: 31779225; PMCID: PMC6928770.

Oleari R, Caramello A, Campinoti S, Lettieri A, Ioannou E, Paganoni A, Fantin A, Cariboni A, Ruhrberg C. PLXNA1 and PLXNA3 cooperate to pattern the nasal axons that guide gonadotropin-releasing hormone neurons. Development. 2019 Nov 5;146(21):dev176461. doi: 10.1242/dev.176461. PMID: 31690636.

Adorni MP, Zimetti F, Cangiano B, Vezzoli V, Bernini F, Caruso D, Corsini A, Sirtori CR, Cariboni A, Bonomi M, Ruscica M. High-Density Lipoprotein Function Is Reduced in Patients Affected by Genetic or Idiopathic Hypogonadism. J Clin Endocrinol Metab. 2019 Aug 1;104(8):3097-3107. doi: 10.1210/jc.2018-02027. PMID: 30835274.

Oleari R, Lettieri A, Paganoni A, Zanieri L, Cariboni A. Semaphorin Signaling in GnRH Neurons: From Development to Disease. Neuroendocrinology. 2019;109(3):193-199. doi: 10.1159/000495916. Epub 2018 Dec 2. PMID: 30504719.

Howard SR, Oleari R, Poliandri A, Chantzara V, Fantin A, Ruiz-Babot G, Metherell LA, Cabrera CP, Barnes MR, Wehkalampi K, Guasti L, Ruhrberg C, Cariboni A, Dunkel L. HS6ST1 Insufficiency Causes Self-Limited Delayed Puberty in Contrast With Other GnRH Deficiency Genes. J Clin Endocrinol Metab. 2018 Sep 1;103(9):3420-3429. doi: 10.1210/jc.2018-00646. PMID: 29931354; PMCID: PMC6126894.

Macchi C, Steffani L, Oleari R, Lettieri A, Valenti L, Dongiovanni P, Romero-Ruiz A, Tena-Sempere M, Cariboni A, Magni P, Ruscica M. Iron overload induces hypogonadism in male mice via extrahypothalamic mechanisms. Mol Cell Endocrinol. 2017 Oct 15;454:135-145. doi: 10.1016/j.mce.2017.06.019. Epub 2017 Jun 23. PMID: 28648620.

Azzarelli R, Oleari R, Lettieri A, Andre’ V, Cariboni A. In Vitro, Ex Vivo and In Vivo Techniques to Study Neuronal Migration in the Developing Cerebral Cortex. Brain Sci. 2017 Apr 27;7(5):48. doi: 10.3390/brainsci7050048. PMID: 28448448; PMCID: PMC5447930.

Howard SR, Guasti L, Ruiz-Babot G, Mancini A, David A, Storr HL, Metherell LA, Sternberg MJ, Cabrera CP, Warren HR, Barnes MR, Quinton R, de Roux N, Young J, Guiochon-Mantel A, Wehkalampi K, André V, Gothilf Y, Cariboni A, Dunkel L. IGSF10 mutations dysregulate gonadotropin-releasing hormone neuronal migration resulting in delayed puberty. EMBO Mol Med. 2016 Jun 1;8(6):626-42. doi: 10.15252/emmm.201606250. PMID: 27137492; PMCID: PMC4888853.

Lettieri A, Oleari R, Gimmelli J, André V, Cariboni A. The role of semaphorin signaling in the etiology of hypogonadotropic hypogonadism. Minerva Endocrinol. 2016 Jun;41(2):266-78. Epub 2016 Mar 4. PMID: 26940457.

Bassi I, André V, Marelli F, Vezzoli V, Merlo GR, Cariboni A, Persani L, Gothilf Y, Bonomi M. The zebrafish: an emerging animal model for investigating the hypothalamic regulation of reproduction. Minerva Endocrinol. 2016 Jun;41(2):250-65. Epub 2016 Mar 2. PMID: 26934719.

Maggi R, Cariboni AM, Marelli MM, Moretti RM, Andrè V, Marzagalli M, Limonta P. GnRH and GnRH receptors in the pathophysiology of the human female reproductive system. Hum Reprod Update. 2016 Apr;22(3):358-81. doi: 10.1093/humupd/dmv059. Epub 2015 Dec 29. PMID: 26715597.

Mantoan Ritter L, Macdonald DC, Ritter G, Escors D, Chiara F, Cariboni A, Schorge S, Kullmann DM, Collins M. Lentiviral expression of GAD67 and CCK promoter-driven opsins to target interneurons in vitro and in vivo. J Gene Med. 2016 Jan-Mar;18(1-3):27-37. doi: 10.1002/jgm.2873. PMID: 26824337.

Rattazzi L, Cariboni A, Poojara R, Shoenfeld Y, D’Acquisto F. Impaired sense of smell and altered olfactory system in RAG-1(-∕-) immunodeficient mice. Front Neurosci. 2015 Sep 9;9:318. doi: 10.3389/fnins.2015.00318. PMID: 26441494; PMCID: PMC4563081.

Cariboni A, André V, Davidson K, Parnavelas J. The molecular control of GnRH neuron development. Springerplus. 2015 Jun 12;4(Suppl 1):L46. doi: 10.1186/2193-1801-4-S1-L46. PMID: 27386208; PMCID: PMC4798131.

Cariboni A, André V, Chauvet S, Cassatella D, Davidson K, Caramello A, Fantin A, Bouloux P, Mann F, Ruhrberg C. Dysfunctional SEMA3E signaling underlies gonadotropin-releasing hormone neuron deficiency in Kallmann syndrome. J Clin Invest. 2015 Jun;125(6):2413-28. doi: 10.1172/JCI78448. Epub 2015 May 18. PMID: 25985275; PMCID: PMC4497752.

Rakić S, Kanatani S, Hunt D, Faux C, Cariboni A, Chiara F, Khan S, Wansbury O, Howard B, Nakajima K, Nikolić M, Parnavelas JG. Cdk5 phosphorylation of ErbB4 is required for tangential migration of cortical interneurons. Cereb Cortex. 2015 Apr;25(4):991-1003. doi: 10.1093/cercor/bht290. Epub 2013 Oct 18. PMID: 24142862; PMCID: PMC4380000.

Tillo M, Erskine L, Cariboni A, Fantin A, Joyce A, Denti L, Ruhrberg C. VEGF189 binds NRP1 and is sufficient for VEGF/NRP1-dependent neuronal patterning in the developing brain. Development. 2015 Jan 15;142(2):314-9. doi: 10.1242/dev.115998. Epub 2014 Dec 17. PMID: 25519242; PMCID: PMC4302834.

Cariboni A, Conti L, Andrè V, Aprile D, Zasso J, Maggi R. Establishment of a radial glia-like mouse fetal hypothalamic neural stem cell line (AC1) able to differentiate into neuroendocrine cells. Neurogenesis (Austin). 2014 Jul 28;1(1):e29950. doi: 10.4161/neur.29950. PMID: 28255570; PMCID: PMC5322806.

Network for Central Hypogonadism (Network Ipogonadismo Centrale, NICe) of Italian Societies of Endocrinology (SIE), of Andrology and Sexual Medicine (SIAMS) and of Peadiatric Endocrinology and Diabetes (SIEDP). Kallmann’s syndrome and normosmic isolated hypogonadotropic hypogonadism: two largely overlapping manifestations of one rare disorder. J Endocrinol Invest. 2014 May;37(5):499-500. doi: 10.1007/s40618-014-0063-z. Epub 2014 Apr 9. PMID: 24715232.

Libri DV, Kleinau G, Vezzoli V, Busnelli M, Guizzardi F, Sinisi AA, Pincelli AI, Mancini A, Russo G, Beck-Peccoz P, Loche S, Crivellaro C, Maghnie M, Krausz C, Persani L, Bonomi M; Italian Study Group on Idiopathic Central Hypogonadism (ICH). Germline prokineticin receptor 2 (PROKR2) variants associated with central hypogonadism cause differental modulation of distinct intracellular pathways. J Clin Endocrinol Metab. 2014 Mar;99(3):E458-63. doi: 10.1210/jc.2013-2431. Epub 2013 Nov 25. PMID: 24276467.

Zito A, Cartelli D, Cappelletti G, Cariboni A, Andrews W, Parnavelas J, Poletti A, Galbiati M. Neuritin 1 promotes neuronal migration. Brain Struct Funct. 2014 Jan;219(1):105-18. doi: 10.1007/s00429-012-0487-1. Epub 2012 Dec 5. PMID: 23212301.

Memi F, Abe P, Cariboni A, MacKay F, Parnavelas JG, Stumm R. CXC chemokine receptor 7 (CXCR7) affects the migration of GnRH neurons by regulating CXCL12 availability. J Neurosci. 2013 Oct 30;33(44):17527-37. doi: 10.1523/JNEUROSCI.0857-13.2013. PMID: 24174685; PMCID: PMC3812513.

Jayakody SA, Andoniadou CL, Gaston-Massuet C, Signore M, Cariboni A, Bouloux PM, Le Tissier P, Pevny LH, Dattani MT, Martinez-Barbera JP. SOX2 regulates the hypothalamic-pituitary axis at multiple levels. J Clin Invest. 2012 Oct;122(10):3635-46. doi: 10.1172/JCI64311. Epub 2012 Sep 4. PMID: 22945632; PMCID: PMC3461924.

Cariboni A, Andrews WD, Memi F, Ypsilanti AR, Zelina P, Chedotal A, Parnavelas JG. Slit2 and Robo3 modulate the migration of GnRH-secreting neurons. Development. 2012 Sep;139(18):3326-31. doi: 10.1242/dev.079418. PMID: 22912413; PMCID: PMC3424043.

Chiara F, Badaloni A, Croci L, Yeh ML, Cariboni A, Hoerder-Suabedissen A, Consalez GG, Eickholt B, Shimogori T, Parnavelas JG, Rakić S. Early B-cell factors 2 and 3 (EBF2/3) regulate early migration of Cajal-Retzius cells from the cortical hem. Dev Biol. 2012 May 1;365(1):277-89. doi: 10.1016/j.ydbio.2012.02.034. Epub 2012 Mar 6. PMID: 22421355; PMCID: PMC3368273.

Bonomi M, Libri DV, Guizzardi F, Guarducci E, Maiolo E, Pignatti E, Asci R, Persani L; Idiopathic Central Hypogonadism Study Group of the Italian Societies of Endocrinology and Pediatric Endocrinology and Diabetes. New understandings of the genetic basis of isolated idiopathic central hypogonadism. Asian J Androl. 2012 Jan;14(1):49-56. doi: 10.1038/aja.2011.68. Epub 2011 Dec 5. PMID: 22138902; PMCID: PMC3735150.

Cariboni A, Ruhrberg C. The hormone of love attracts a partner for life. Dev Cell. 2011 Oct 18;21(4):602-4. doi: 10.1016/j.devcel.2011.09.018. PMID: 22014517.

Cariboni A, Davidson K, Dozio E, Memi F, Schwarz Q, Stossi F, Parnavelas JG, Ruhrberg C. VEGF signalling controls GnRH neuron survival via NRP1 independently of KDR and blood vessels. Development. 2011 Sep;138(17):3723-33. doi: 10.1242/dev.063362. PMID: 21828096; PMCID: PMC3152927.

Hernández-Miranda LR, Cariboni A, Faux C, Ruhrberg C, Cho JH, Cloutier JF, Eickholt BJ, Parnavelas JG, Andrews WD. Robo1 regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain. J Neurosci. 2011 Apr 20;31(16):6174-87. doi: 10.1523/JNEUROSCI.5464-10.2011. PMID: 21508241; PMCID: PMC3088089.

Zaninetti R, Fornarelli A, Ciarletta M, Lim D, Caldarelli A, Pirali T, Cariboni A, Owsianik G, Nilius B, Canonico PL, Distasi C, Genazzani AA. Activation of TRPV4 channels reduces migration of immortalized neuroendocrine cells. J Neurochem. 2011 Feb;116(4):606-15. doi: 10.1111/j.1471-4159.2010.07144.x. Epub 2011 Jan 19. PMID: 21166676.

Cariboni A, Davidson K, Rakic S, Maggi R, Parnavelas JG, Ruhrberg C. Defective gonadotropin-releasing hormone neuron migration in mice lacking SEMA3A signalling through NRP1 and NRP2: implications for the aetiology of hypogonadotropic hypogonadism. Hum Mol Genet. 2011 Jan 15;20(2):336-44. doi: 10.1093/hmg/ddq468. Epub 2010 Nov 8. PMID: 21059704.

Zaninetti R, Tacchi S, Erriquez J, Distasi C, Maggi R, Cariboni A, Condorelli F, Canonico PL, Genazzani AA. Calcineurin primes immature gonadotropin-releasing hormone-secreting neuroendocrine cells for migration. Mol Endocrinol. 2008 Mar;22(3):729-36. doi: 10.1210/me.2007-0277. Epub 2007 Nov 21. PMID: 18032695; PMCID: PMC5419618.

Cariboni A, Maggi R, Parnavelas JG. From nose to fertility: the long migratory journey of gonadotropin-releasing hormone neurons. Trends Neurosci. 2007 Dec;30(12):638-44. doi: 10.1016/j.tins.2007.09.002. Epub 2007 Nov 5. PMID: 17981344.

Moretti RM, Montagnani Marelli M, Mai S, Cariboni A, Scaltriti M, Bettuzzi S, Limonta P. Clusterin isoforms differentially affect growth and motility of prostate cells: possible implications in prostate tumorigenesis. Cancer Res. 2007 Nov 1;67(21):10325-33. doi: 10.1158/0008-5472.CAN-07-0516. PMID: 17974975.

Magni P, Dozio E, Ruscica M, Watanobe H, Cariboni A, Zaninetti R, Motta M, Maggi R. Leukemia inhibitory factor induces the chemomigration of immortalized gonadotropin-releasing hormone neurons through the independent activation of the Janus kinase/signal transducer and activator of transcription 3, mitogen-activated protein kinase/extracellularly regulated kinase 1/2, and phosphatidylinositol 3-kinase/Akt signaling pathways. Mol Endocrinol. 2007 May;21(5):1163-74. doi: 10.1210/me.2006-0270. Epub 2007 Feb 13. PMID: 17299136.

Cariboni A, Hickok J, Rakic S, Andrews W, Maggi R, Tischkau S, Parnavelas JG. Neuropilins and their ligands are important in the migration of gonadotropin-releasing hormone neurons. J Neurosci. 2007 Feb 28;27(9):2387-95. doi: 10.1523/JNEUROSCI.5075-06.2007. PMID: 17329436; PMCID: PMC6673474.

Cariboni A, Maggi R. Kallmann’s syndrome, a neuronal migration defect. Cell Mol Life Sci. 2006 Nov;63(21):2512-26. doi: 10.1007/s00018-005-5604-3. PMID: 16952059.

Cariboni A, Rakic S, Liapi A, Maggi R, Goffinet A, Parnavelas JG. Reelin provides an inhibitory signal in the migration of gonadotropin-releasing hormone neurons. Development. 2005 Nov;132(21):4709-18. doi: 10.1242/dev.02033. Epub 2005 Oct 5. PMID: 16207762.

Maggi R, Cariboni A, Zaninetti R, Samara A, Stossi F, Pimpinelli F, Giacobini P, Consalez GG, Rugarli E, Piva F. Factors involved in the migration of neuroendocrine hypothalamic neurons. Arch Ital Biol. 2005 Sep;143(3-4):171-8. PMID: 16097493.

Dondi D, Piccolella M, Messi E, Demissie M, Cariboni A, Selleri S, Piva F, Samara A, Consalez GG, Maggi R. Expression and differential effects of the activation of glucocorticoid receptors in mouse gonadotropin-releasing hormone neurons. Neuroendocrinology. 2005;82(3-4):151-63. doi: 10.1159/000091693. Epub 2006 Feb 22. PMID: 16498266.

Cariboni A, Pimpinelli F, Colamarino S, Zaninetti R, Piccolella M, Rumio C, Piva F, Rugarli EI, Maggi R. The product of X-linked Kallmann’s syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum Mol Genet. 2004 Nov 15;13(22):2781-91. doi: 10.1093/hmg/ddh309. Epub 2004 Oct 7. PMID: 15471890.

Cariboni A. Microtubules in mouse neurons. Nat Cell Biol. 2004 Oct;6(10):929. doi: 10.1038/ncb1004-929. PMID: 15459721.

Pimpinelli F, Redaelli E, Restano-Cassulini R, Curia G, Giacobini P, Cariboni A, Wanke E, Bondiolotti GP, Piva F, Maggi R. Depolarization differentially affects the secretory and migratory properties of two cell lines of immortalized luteinizing hormone-releasing hormone (LHRH) neurons. Eur J Neurosci. 2003 Sep;18(6):1410-8. doi: 10.1046/j.1460-9568.2003.02866.x. PMID: 14511321.

Giacobini P, Giampietro C, Fioretto M, Maggi R, Cariboni A, Perroteau I, Fasolo A. Hepatocyte growth factor/scatter factor facilitates migration of GN-11 immortalized LHRH neurons. Endocrinology. 2002 Sep;143(9):3306-15. doi: 10.1210/en.2002-220146. PMID: 12193542.