Editorial: Parvoviruses: from basic research to biomedical and biotechnological applications

TYPE Edi o ial PUBLISHED 15 May 2023 DOI 10.3389/ micb.2023.1194926 OPEN ACCESS EDITED AND REVIEWED BY Anna K am is, Uni e si y o he Wi wa e s and, Sou h A ica *CORRESPONDENCE Ma ia Söde lund-Vene mo ma ia.sode lund- ene mo@helsinki.fi RECEIVED 27 Ma ch 2023 ACCEPTED 28 Ap il 2023 PUBLISHED 15 May 2023 CITATION Mie zsch M, Qiu J, Almend al JM and Söde lund-Vene mo M (2023) Edi o ial: Pa o i uses: om basic esea ch o biomedical and bio echnological applica ions. F on . Mic obiol. 14:1194926. doi: 10.3389/ micb.2023.1194926 COPYRIGHT ©2023 Mie zsch, Qiu, Almend al and Söde lund-Vene mo. This is an open-access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License (CC BY). The use, dis ibu ion o ep oduc ion in o he o ums is pe mi ed, p o ided he o iginal au ho (s) and he copy igh owne (s) a e c edi ed and ha he o iginal publica ion in his jou nal is ci ed, in acco dance wi h accep ed academic p ac ice. No use, dis ibu ion o ep oduc ion is pe mi ed which does no comply wi h hese e ms. Edi o ial: Pa o i uses: om basic esea ch o biomedical and bio echnological applica ions Ma io Mie zsch1, Jianming Qiu2, José M. Almend al3and Ma ia Söde lund-Vene mo4* 1Depa men o Biochemis y and Molecula Biology, Uni e si y o Flo ida, Gaines ille, FL, Uni ed S a es, 2Depa men o Mic obiology, Molecula Gene ics and Immunology, Uni e si y o Kansas Medical Cen e , Kansas Ci y, KS, Uni ed S a es, 3Cen o de Biología Molecula Se e o Ochoa, Depa amen o de Biología Molecula , Uni e sidad Au ónoma de Mad id, Mad id, Spain, 4Depa men o Vi ology, Uni e si y o Helsinki, Helsinki, Finland KEYWORDS pa o i us B19, human boca i us, adeno-associa ed i us, minu e i us o mice, eline chaphamapa o i us, pa o i us Edi o ial on he Resea ch Topic Pa o i uses: om basic esea ch o biomedical and bio echnological applica ions Pa o i uses a e small non-en eloped icosahed al i uses wi h linea single-s anded DNA genomes o 4–6 kb wi h e minal epea s o ming hai pin s uc u es a bo h ends. To da e, he amily Pa o i idae comp ises h ee sub amilies; Pa o i inae,Denso i inae, and Hamapa o i inae, wi h i us membe s in ec ing ei he e eb a e o in e eb a e hos s, o bo h, espec i ely (Pénzes e al., 2020). Pa o i us eplica ion is highly dependen on hos cell ac o s, including DNA polyme ases. Thei eplica ion mos ly akes place in ac i ely di iding cells bu some imes also in quiescen cells. Pa o i uses cause subclinical o deadly in ec ions and o en pe sis in he hos wi h unknown consequences. Some pa o i uses, like H-1, a e used as oncoly ic i uses o cance ea men , and o he s as ec o s o gene he apy, like he adeno-associa ed i uses (AAVs) (Angelo a e al., 2021;Pupo e al., 2022). The mos widely known pa o i us pa hogens o humans a e pa o i us B19 (B19V) and human boca i us 1 (HBoV1) (Qiu e al., 2017), and o animals, e.g., he canine, mink, bo ine, and po cine pa o i uses, o which accines a e a ailable, and minu e i us o mice (MVM), which has been mos widely s udied (Figu e 1;Jage e al., 2021). Many denso i uses a e highly pa hogenic o insec s o c us aceans, and some a e being used o pes con ol (Johnson and Rasgon, 2018). This Resea ch Topic ocuses on he ecen ad ances ac oss he en i e spec um o molecula , clinical, and applied pa o i us esea ch. In he opic o pa o i us — cell-su ace in e ac ion, La ge and Chapman e isi ed he p e iously epo ed capsid- ecep o complex s uc u es o he AAVs and compa ed hei binding si es o he epi opes o neu alizing an ibodies. The au ho s sugges ed ha he p o einaceous AAV Recep o (AAVR), KIAA0319L, is one o he main con ibu o s o cellula ansduc ion, while he cell su ace glycans should be demo ed o a achmen ac o s, and he iden i ied co- ecep o s only ha e mino accesso y oles. They concluded ha an ibody in e e ence wi h AAVR binding migh be a mo e p e alen mechanism o AAV neu aliza ion a he han he in e e ence wi h glycan a achmen . F on ie s in Mic obiology 01 on ie sin.o g Mie zsch e al. 10.3389/ micb.2023.1194926 The ole o pa o i us-glycan in e ac ion in he in ec ion may, howe e , di e be ween pa o i us sys ems. Fo ins ance, su ace glycans, as unc ional ecep o s, d i ing i ion en y was epo ed by Cal o-López e al., while e a ge ing he p o opa o i us MVM o he umo ascula u e wi h ascula endo helial g ow h ac o (VEGF) blocking pep ides inse ed a he sialic acid (sia) binding domain nea he 2- old axis. The MVM-VEGF chime ic i ion showed al e ed opism de e mined by capsid con ac s wi h cell- ype speci ic sia glycans d i ing he i ion o he endosome, whe e a d as ic s uc u al ansi ion onse s p oduc i e en y. In addi ion, he sia-dependen en y could be u he enhanced by con olled neu aminidase ea men s. The iden i ica ion o he in acellula a ic o he endosome as a key s ep o MVM en y may help unde s anding he opism and hos ange o o he pa o i uses. O he opics o in e es add essed he in e ac ion o a pa hogenic pa o i us wi h mammalian hos s in na u e. By mode n me agenomics, many no el eme ging pa o i uses ha e been disco e ed, like he eline chaphamapa o i us (FeChPV) in 2019 (Li e al., 2020). Hao e al. epo ed pa hogenic ea u es o an ou b eak o FeChPV in China. They showed se e e symp oms in he uppe espi a o y ac , se e e lymphadeni is and encephali is co esponding o he p esence o i al DNA in he eline issues. FIGURE 1 The icosahed al capsids o selec ed pa o i uses o human [adeno-associa ed i us 2 ( op), pa o i us B19 (bo om)], cow (bo ine pa o i us), mouse (minu e i us o mice), sh imp (Penaeus monodon me allodenso i us), and mo h (Galle ia mellonella denso i us) a e shown. Illus a ion designed by Jane Hsi. In e es ingly, i al p o ein (VP) 1 showed se en and he non- s uc u al p o ein 1 eigh unique amino-acid mu a ions, he oles o which, in he pa hogenici y o he i us, dese e u he esea ch. Human pa o i us B19 was long he only known human- pa hogenic pa o i us, causing e y hema in ec iosum, a h opa hies, anemias, and e al dea h (Qiu e al., 2017), whe eas HBoV1, causing pedia ic mild o li e- h ea ening acu e espi a o y- ac in ec ions (ARTI), was disco e ed in 2005 (Allande e al., 2005;Ch is ensen e al., 2019). Xu e al. sea ched o pa o i al DNA in a o al o 427 in es inal biopsy specimens, as pai ed diseased and heal hy mucosa. Only h ee (1.6%) indi iduals exhibi ed in es inal HBoV DNA, compa ed o 50, 47, 31, and 27% o pa ien s wi h malignancy, ulce a i e coli is, o adenomas, and in heal hy subjec s, espec i ely, who ha bo ed B19V DNA. B19V DNA pe sis ed mos ly in he mucosal B cells o lymphoid ollicles and in ascula endo helial cells. When compa ing B19V DNA-posi i e and -nega i e heal hy ileum biopsy specimens, RNA sequencing iden i ied 272 di e en ially exp essed cellula genes, which ac i a ed in es inal cell iabili y and inhibi ed apop osis. B19V-DNA pe sis ence was hus shown o modula e hos gene exp ession, wi h ye unknown clinical ou comes. F on ie s in Mic obiology 02 on ie sin.o g Mie zsch e al. 10.3389/ micb.2023.1194926 The e we e wo s udies o HBoV1 om China. De e al. sc eened espi a o y specimens om child en wi h ARTI by h ee me hods. Ou o 9,899 ai way samples, 681 (7%) we e posi i e o HBoV1 DNA by a capilla y elec opho esis-based mul iplex PCR (CEMP) assay, 37/47 samples es ed exhibi ed HBoV1-VP3 an igen by indi ec -immuno luo escence assay (IFA), and HBoV1-speci ic IgG was es ed by IFA o ou pa ien s wi h a ailable pai ed se a. They concluded ha he combina o ial esul s o DNA, an igen, and se ology es s a e p oo o HBoV1 being a genuine pa hogen o ARTI in child en. Wang e al. e alua ed he p e alence, epidemiology, and clinical cha ac e is ics o HBoV among child en wi h ARTI. They sc eened nasopha yngeal swabs o 16 i al and 16 bac e ial pa hogens by wo mul iplex PCRs, and compa ed clinical pa ame e s in a ious g oups. HBoV1 was he mos common i us (56/199, 28.1%) and he second mos common pa hogen de ec ed, a e S. pneumoniae (71/199, 35.7%). Fo y- wo (75%) cases we e HBoV1 single- i us in ec ions and 14 (25%) we e HBoV single- pa hogen in ec ions. Vomi ing o dia hea was de ec ed in i e child en in he sole-HBoV g oup s. none in he coin ec ion g oup, bu he la e g oup exhibi ed a highe p opo ion o wheezing. In pa o i us gene he apy app oaches, Sho i e al. upda ed he manu ac u ing p o ocol o a no el no-end (NE) AAV DNA ha consis s o a gene exp ession casse e co alen ly lanked by AAV2 in e ed e minal epea s (ITRs), and assessed a ious NE-AAV DNA o ms in immo alized hepa ocy e cell lines by ans ec ion. Finally, hey de eloped an NE-AAV DNA ha has a human Fac o IX (hF.IX) gene exp ession casse e unde he con ol o a human li e -speci ic ans hy e in p omo e , and p o ed i o exp ess, in human hepa ocy e cells a ou -weeks pos - ans ec ion, ∼6- old highe le els o hF.IX han ha om a linea TTR-hF.IX DNA cons uc . This no el NE AAV DNA opens ano he enue o gene he apy o hemophilia in child en. Au ho con ibu ions All au ho s lis ed ha e made a subs an ial, di ec , and in ellec ual con ibu ion o he wo k and app o ed i o publica ion. Conflic o in e es The au ho s decla e ha he esea ch was conduc ed in he absence o any comme cial o inancial ela ionships ha could be cons ued as a po en ial con lic o in e es . Publishe ’s no e All claims exp essed in his a icle a e solely hose o he au ho s and do no necessa ily ep esen hose o hei a ilia ed o ganiza ions, o hose o he publishe , he edi o s and he e iewe s. Any p oduc ha may be e alua ed in his a icle, o claim ha may be made by i s manu ac u e , is no gua an eed o endo sed by he publishe . Re e ences Allande , T., Tammi, M. T., E iksson, M., Bje kne , A., Ti eljung-Lindell, A., and Ande sson, B. (2005). Cloning o a human pa o i us bymolecula sc eening o espi a o y ac samples. P oc. Na l. Acad. Sci. U. S. A. 102, 12891–12896. doi: 10.1073/pnas.0504666102 Angelo a, A., Fe ei a, T., B e sche , C., Rommelae e, J., and Ma chini, A. (2021). Pa o i us-based combina o ial immuno he apy: a ein o ced he apeu ic s a egy agains poo -p ognosis solid cance s. Cance s 13, 342. doi: 10.3390/cance s130 20342 Ch is ensen, A., Kes i, O., Elenius, V., Eskola, A. L., Døllne , H., Al unbulakli, C., e al. (2019). Human boca i uses and paedia ic in ec ions. Lance Child Adolesc. Heal h 3, 418–426. doi: 10.1016/S2352-4642(19)3 0057-4 Jage , M. C., Tomlinson, J. E., Lopez-As acio, R. A., Pa ish, C. R., and Van de Walle, G. R. (2021). Small bu migh y: old and new pa o i uses o e e ina y signi icance. Vi ol. J. 18, 210. doi: 10.1186/s12985-021-01677-y Johnson, R. M., and Rasgon, J. L. (2018). Densonucleosis i uses (“denso i uses”) o mosqui o and pa hogen con ol. Cu . Opin. Insec Sci. 28, 90–97. doi: 10.1016/j.cois.2018.05.009 Li, Y., Go don, E., Idle, A., Al an, E., Seguin, M. A., Es ada, M., e al. (2020). Vi ome o a eline ou b eak o dia hea and omi ing includes boca i uses and a no el chappa o i us. Vi uses 12, 506. doi: 10.3390/ 12050506 Pénzes, J. J., Söde lund-Vene mo, M., Canu i, M., Eis-Hübinge , A. M., Hughes, J., Co mo e, S. F., e al. (2020). Reo ganizing he amily Pa o i idae: a no el axonomy independen om he canonical app oach based on hos a ilia ion. A ch. Vi ol. 165, 2133–2146. doi: 10.1007/s00705-020-04632-4 Pupo, A., Fe nández, A., Low, S. H., F ançois, A., Suá ez-Ama án, L., and Samulski, R. J. (2022). AAV ec o s: he Rubik’s cube o human gene he apy. Mol. The . 30, 3515–3541. doi: 10.1016/j.ym he.2022.09.015 Qiu, J., Söde lund-Vene mo, M., and Young, N. S. (2017). Human pa o i uses. Clin. Mic obiol. Re . 30, 43–113 doi: 10.1128/CMR.00040-16 F on ie s in Mic obiology 03 on ie sin.o g