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  • ReceivedMar 9, 2020
  • AcceptedMar 21, 2020
  • PublishedJul 2, 2020

Abstract


Acknowledgment

This work was supported by a grant from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA16040201). The authors thank Mrs. Meiyuan Xing and Mr. Haifeng Tu for the development of literature search strategy and conducting the actual search. They also thank Dr. Yuxi Zheng, Dr. Hong Zhu, Dr. Mengyun Liu, Dr. Liyue Zhang, and Dr. Qianjie Yang (Department of Ophthalmology, First Affiliated Hospital, College of Medicine, Zhejiang University) for their help in information gathering and useful discussion. The strong technical support from Mr. Tang-liang Jiang during the development of the manuscript is deeply appreciated.


Interest statement

The author(s) declare that they have no conflict of interest.


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  • Figure 1

    The scope of regenerative ophthalmology.

  • Figure 2

    Corneal regeneration from limbal stem cells.

  • Figure 3

    The sketch of RPE transplantation.

  • Figure 4

    Technology and application of corneal lenticules: a flow chart.

  • Figure 5

    Bioengineering applied to cell and tissue manufacture and delivery (from Stern et al., 2018).

  • Table 1   Collagen application in corneal tissue engineering

    Form

    Description/scheme

    Key advantages

    Key disadvantages

    Notes

    Collagenhydrogels

    Gels built by a network of fibrillar collagen

    Classical approach

    Unsatisfactory robustness

    Crosslinkedcollagen hydrogel

    Gels built by a network of fibrillar collagen, crosslinked

    Resistant to enzymatic digestion

    Superior mechanical properties

    Epithelial regeneration

    *Molding or 3D printing in layers

    Sponges

    Porous network of collagen fibrils

    Porosity for cell penetration

    High light transmittance

    Superior mechanical properties

    Favored for stromal matrix regeneration overhydrogels

    Films

    Crosslinkedas thin sheets of collagen fibrils (typical thickness <100 mm)

    High transparency

    Superior mechanical properties

    Limited cellpenetration

    Augmentedcollagen

    Collagenmatrix, typically type-I collagensupplemented with proteoglycans and polysaccharides/polylipids

    Mimics biological and in vivo composition of the corneal stroma

    High transparency

     

  • Table 2   Summary of recent application of gelatin in regenerative ophthalmologya)

    Part of the eye

    Methods (formulation)

    Applications

    Types of study

    Species

    References

    Ocular surface

    3D-printed membrane based on gelatin, elastin, and sodium HA blend

    Conjunctival defectreconstruction

    In vitro &

    in vivo

    Rabbit

    (Dehghani et al., 2018)

    Cornea

    Epithelial and limbal stem cells

    Carboxymethyl chitosan/gelatin/HA-blended membranes

    Corneal wound healing

    In vitro &

    in vivo

    Rabbit

    (Xu et al., 2018)

    Crosslinked collagen/gelatin/HA biomimetic film

    Cornea tissue engineering

    In vitro

    Human

    (Liu et al., 2013)

    Electrospun gelatin fiber-alginate gel

    Cornea tissue engineering

    In vitro

    Porcine

    (Tonsomboon and Oyen, 2013)

    Electrospun gelatin mat

    Cornea tissue engineering

    In vitro

    Human

    (Momenzadeh et al., 2017)

    Photocurable gelatin scaffold

    Repair of focal corneal wounds

    In vivo

    Rabbit

    (Li et al., 2018)

    Stroma

    Crosslinked gelatin

    Treatment for corneal stroma

    In vitro &

    in vivo

    Rabbit

    (Mimura et al., 2008)

    Gelatin/ascorbic acid cryogel carriers

    Corneal stroma reconstruction

    In vitro &

    in vivo

    Rabbit

    (Luo et al., 2018)

    Keratocyte-loaded methacrylated gelatin hydrogels

    Mimicking corneal stroma

    In vitro

    Human

    (Kilic Bektas and Hasirci, 2018)

    Gelatin/chondroitin sulfate scaffolds

    Corneal stromal tissueengineering

    In vitro

    Rabbit

    (Lai, 2013b)

    Endothelium

    Gelatin carrier

    Corneal endothelial celltransplantation

    In vitro &

    in vivo

    Rabbit & human

    (Lai et al., 2006; Lai et al., 2007)

    Heparin-modified gelatinscaffolds

    Corneal endothelial celltransplantation

    In vitro &in vivo

    Human & rabbit

    (Niu et al., 2014)

    Lens

    Gelatin microbeads

    Ocular lens development

    In vitro

    Mouse

    (Wang and Han, 2017)

    Retina

    Retinal pigment epithelium

    Gelatin membrane RPE sheet carrier

    Retinal sheet transplantation

    In vitro &

    in vivo

    Rabbit

    (Hsiue et al., 2002)

    Electrospun RWSF/PCL/gelatin substrate scaffold

    RPE transplantation

    In vitro &

    in vivo

    Human & rabbit

    (Xiang et al., 2014)

    Poly(ε-caprolactone)/gelatinnanofibrous scaffolds

    RPE regeneration

    In vitro

    Human

    (Rahmani et al., 2018)

    Electrospun thin gelatin/chitosan nanofibrous scaffolds

    RPE regeneration

    In vitro

    Human

    (Noorani et al., 2018)

    Retinal progenitor cells

    In situ crosslinked injectable gelatin-HPA hydrogel

    RPC transplantation

    In vitro &in vivo

    Human & rat

    (Park et al., 2019)

    Retinal tears

    Gelatin-mTG complex

    Retinal detachment repair

    In vivo

    Rat

    (Yamamoto et al., 2013)

    Injectable gelatin-HA hydrogels

    Differentiation of retinalprogenitor cells

    In vitro

    Human

    (Tang et al., 2019)

    HA, hyaluronic acid/hyaluronate; RPE, retinal pigment epithelium; RWSF, Antheraeapernyi silk fibroin; PCL, polycaprolactone; HPA, hydroxyphenyl propionic acid; RPC, retinal progenitor cells; mTG, microbial transglutaminase.

  • Table 3   Summary of recent applications of ADSCs in regenerative ophthalmologya)

    Part of the eye

    Indication for application*

    Types of study

    Species

    References

    Cornea

    Epithelium or

    limbal stem cells (LSCs)

    Laser-induced corneal wounds

    In vivo

    Mouse

    (Zeppieri et al., 2017)

    Corneal chemical burn

    In vivo

    Rabbit & rat

    (Lin et al., 2013; Zeppieri et al., 2013)

    Scleral contact lens carrier in alkali burn

    In vivo

    Rabbit

    (Espandar et al., 2014)

    LSC deficiency

    In vivo

    Rabbit

    (Sun et al., 2017)

    LSC niche damage

    In vivo

    Rabbit

    (Galindo et al., 2017)

    Corneal stroma

    Differentiate into keratocytes

    In vitro

    Human

    (Du et al., 2010)

    Differentiate into keratocytes

    In vitro

    Human

    (Dos Santos et al., 2019)

    Endothelium

    Change to CEC

    In vitro

    Human

    (Chen et al., 2014)

    Corneal endothelial dysfunction

    In vivo

    Rat & monkey

    (Sun et al., 2017)

    Retina

    Diabetic retinopathy

    Improve the blood–retinal barrier function

    In vivo

    Rat

    (Mendel et al., 2013)

    Trigger a cytoprotective microenvironment

    In vivo

    Mouse

    (Ezquer et al., 2016)

    Control of early retinal complications

    In vivo

    Mouse

    (Barber et al., 2005)

    Ameliorate DR-related gene expression

    In vivo

    Mouse

    (Elshaer et al., 2018)

    AMD & RP

    Promote RPC differentiation into neurons

    In vitro

    Mouse

    (Ji et al., 2018)

    Protect and rescue RPE

    In vivo

    Mouse

    (Barzelay et al., 2018)

    Promote differentiation into retinal pigment epithelial cells

    In vitro

    Human

    (Aboutaleb Kadkhodaeian et al., 2019)

    Retinal hole

    Retinal hole recovery

    In vivo

    Rabbit

    (Xuqian et al., 2011)

    Other parts of the eye

    Orbital fat

    Orbital volume deficiency

    In vivo

    Rabbit

    (Lee et al., 2013)

    Lacrimal gland

    Autoimmune dacryoadenitis

    In vivo

    Rabbit

    (Liu, 2017)

    CEC, corneal endothelial-like cells; AMD, age-related macular degeneration; RP, retinitis pigmentosa; RPC, retinal progenitor cells; RPE, retinal pigmented epithelium.*, in vivo studies; we report the condition in which ADSCs were used to achieve tissue repair, whereas for in vitro studies, we report the main effect of ADSC on ocular tissues/cells.

  • Table 4   Summary of recent applications of MSCs, LSCs and EpiSCs in regenerative ophthalmologya)

    Types of stem cells

    Applications

    Types of study

    Species

    References

    MSCs

    Corneal alkali burns

    In vivo

    Rabbit

    (Cejka et al., 2016)

    Corneal alkali burns

    In vivo

    Rat

    (Ke et al., 2015)

    Corneal alkali burns

    In vivo

    Rabbit

    (Holan et al., 2015)

    Corneal alkali burns

    In vivo

    Rat

    (Acar et al., 2015)

    Corneal regeneration

    In vitro

    Human

    (Dos Santos et al., 2019)

    Dry eye disease

    In vivo

    Mice

    (Lee et al., 2015)

    Dry eye disease

    In vivo

    Rat

    (Beyazyıldız et al., 2014)

    Degenerative retinal diseases

    In vivo

    Rat

    (Choi et al., 2016)

    LSCs

    Limbal stem cell deficiency

    In vivo

    Human

    (Daya et al., 2005)

    Limbal stem cell deficiency following ocular burns

    In vivo

    Human

    (Sangwan et al., 2012)

    Limbal stem cell deficiency following ocular burns

    In vivo

    Human (children)

    (Mittal et al., 2016)

    Limbal stem cell deficiency following ocular burns

    In vivo

    Human

    (Gupta et al., 2018)

    Limbal stem cell deficiency following ocular burns

    In vivo

    Human

    (Pellegrini et al., 1997)

    Limbal stem cell deficiency following ocular burns

    In vivo

    Human

    (Rama et al., 2010)

    EpiSC

    Total limbal stem cell deficiency

    In vivo

    Goat

    (Yang et al., 2008)

    In vitro corneal differentiation protocol*

    In vitro

    Human

    (Ouyang et al., 2014)

    Corneal damage

    In vitro

    Human

    (Saichanma et al., 2012)

    MSCs, mesenchymal stem cells; LSCs, limbal stem cells; EpiSC, epidermal stem cells.

  • Table 5   Summary of clinical trials on stem cell application for retinal regenerationa)

    Trials

    Status

    Disease(s)

    Completion date or estimate

    Participants

    Phase

    Trial number*

    Subretinal hESC-RPE

    Completed

    Stargardt’s disease

    August 2015

    13

    I, II

    NCT01345006

    Subretinal hESC-RPE

    Completed

    Dry AMD

    August 2015

    18

    I, II

    NCT01344993

    Subretinal hESC-RPE

    Completed

    Stargardt’s disease

    September 2015

    12

    I, II

    NCT01469832

    Intravitreal BMSC

    Completed

    AMD and Stargartd’s disease

    December 2015

    20

    N/A

    NCT01518127

    Intravitreal BMSC

    Completed

    Retinal degeneration, POAG

    September 2016

    2

    I

    NCT02330978

    Subretinal HuCNS-SC cells

    Completed

    AMD

    June 2015

    15

    I, II

    NCT01632527

    Subretinal SCNT-hES-RPE

    Enrolling byinvitation

    Dry AMD

    April 2019

    3

    I

    NCT03305029

    Subretinal hESC-RPE

    Unknown

    Outer retinal degenerations

    June 2019

    18

    I, II

    NCT02903576

    Subretinal hESC-RPE

    Active, not recruiting

    Acute wet AMD

    December 2019

    2

    I

    NCT01691261

    Intravitreal BM-SC

    Enrolling byinvitation

    Retinal degenerative diseases

    March 2020

    30

    I

    NCT03772938

    Intravitreal jCell

    Active, not recruiting

    Retinitis pigmentosa

    January 2021

    84

    II

    NCT03073733

    Subretinal hESC-RPE

    Active, not recruiting

    Advanced dry AMD

    June 2023

    16

    I, II

    NCT02590692

    Retrobulbar, subtenon,intravitreal, intraocular, subretinal and intravenous BMSC

    Recruiting

    Retinal and optic nervedamage or disease

    January 2021

    500

    N/A

    NCT03011541

    hESC-RPE, human embryonic stem cell-derived retinal pigment epithelium; BMSC, bone marrow-derived stem/progenitor cell (unspecified); BM-MSC, bone marrow-derived mesenchymal stem cells; AMD, age-related macular degeneration; POAG, primary open-angle glaucoma; HuCNS-SC cells, human central nervous system stem cells; jCell, retinal progenitor cells; SCNT-hES-RPE, human somatic cell nuclear transfer embryonic stem cell-derived retinal pigmented epithelium.*, All trials are listed as per the trial number on ClinicalTrials.gov database maintained by the U.S. National Library of Medicine.

  • Table 6   Summary of recent applications of corneal lenticules

    Categories

    Applications

    Freshness and source of the lenticule

    Species

    Number ofpatients/eyes

    References

    Testing FILIprocedure

    Restore stromal volume afterrefractive lenticule extraction

    Autologous

    Rabbit

    6/6

    (Angunawela et al., 2012)

    Testing FILI procedure

    Fresh/immediately derived from the contralateral eye

    Rabbit

    15/15

    (Zhang et al., 2015)

    Testing FILI procedure

    Cryopreserved for 3 months

    Rabbit

    20/20

    (Sun et al., 2016)

    Treatment of refractive anomalies

    Hyperopia treatment

    Fresh/immediately derived from the other myopic eye

    Human

    5/5

    (Sun et al., 2015)

    Hyperopia, presbyopia, andkeratoectasiatreatment

    Fresh/immediately derived from a donor

    Monkey

    3/4

    (Liu et al., 2015)

    Presbyopia treatment

    Allogenic

    Human

    4/4

    (Jacob et al., 2017)

    Hyperopia treatment

    Derived from a myopic donor, stored

    Human

    1/1

    (Pradhan et al., 2013)

    Hyperopia and aphakia treatment

    Stored, cryopreserved forapproximately 3 months

    Human

    9/9

    (Ganesh et al., 2014)

    Use as a patch

    Closing exposed Ahmed glaucoma valve tube and bullous keratopathy

    Immediately derived from adonor

    Human

    3/3

    (Song et al., 2018)

    Treating recurrence of cornealdystrophy

    Allogenic

    Human

    6/6

    (Zhao et al., 2016)

    Treating recurrent pterygiumcomplicated by a thin cornea

    Immediately derived from adonor

    Human

    1/1

    (Pant et al., 2018)

    Treating corneal ulcer and corneal perforation

    From a donor

    Human

    20/22

    (Jiang et al., 2016)

    Treating limbal dermoids

    From a donor

    Human

    1/1

    (Pant et al., 2018)

    Treating macroperforations after DALK

    From a donor

    Human

    1/1

    (Jacob et al., 2019)

    Treatment ofkeratoconus

    Treating progressive keratoconus

    Cryopreserved, derived from a donor

    Human

    6/6

    (Ganesh and Brar, 2015)

    Treating stage III and IV stable keratoconus

    From a corneoscleral eye bank

    Human

    10/10

    (Mastropasqua et al., 2018)

    Treating progressive stage II–III keratoconus

    Donor tissues from an eye bank

    Human

    11/11

    (Jin et al., 2019)

    Treating advancedkeratoconus

    From a donor

    Human

    1/1 (child)

    (Almodin et al., 2018)

    Treating post-LASIK corneal ectasia

    From a donor

    Human

    1/1

    (Li et al., 2018)

  • Table 7   Summary of recent application of smart biomaterials in ocular drug deliverya)

    Materials

    Drugs

    Applications

    Types of study/species

    References

    Hydroxypropyl trimethyl ammonium chloride CS-based TS hydrogel

    Dexamethasone

    Inflammation

    In vitro

    (Tan et al., 2017)

    TS smart polymer

    Dexamethasone

    Uveitis

    Rabbit

    (Rafie et al., 2010)

    Biodegradable TS PLGA–PEG–PLGApolymer

    In vitro

    (Chan et al., 2019)

    Mucoadhesive polymer-based ocularmicrospheres

    Ganciclovir

    HSV keratitis and CMV retinitis

    Rat

    (Kapanigowda et al., 2015)

    SS hydrogels based on polyacrylic acid

    Ofloxacin

    External infections of the eye

    In vitro

    (Patel et al., 2012)

    SS hydrogels based on polyacrylic acid

    Timolol maleate andbrimonidine tartrate

    Glaucoma

    Rabbit

    (Dubey and Prabhu, 2014)

    IS sodium alginate hydrogel

    Moxifloxacin hydrochloride

    Eye infections

    In vitro, rabbit

    (Mandal et al., 2012)

    IS gelrite/alginate system

    Alkaloid marine

    Eye inflammation

    In vitro, rabbit, human

    (Liu et al., 2010)

    Electrically controlled delivery system using polypyrrole

    Dexamethasone

    AMD, DME

    In vitro

    (Ramtin et al., 2016)

    Sodium alginate hydrogel, polyox hydrogel, and poloxamer hydrogel

    Moxifloxacinhydrochloride

    Eye infections

    In vitro, rabbit

    (Nanjwade et al., 2012)

    NS lipid carrier-based dual stimulus-responsive hydrogels of TS polymer Pluronic F127 (PF127) and pH-responsive polymer CS

    Ibuprofen

    Inflammation

    In vitro

    (Almeida et al., 2016)

    NS lipid carrier-based pH and temperature DR hydrogel composed of carboxymethyl CS and poloxamer

    Quercetin

    Inflammation

    In vitro

    (Yu et al., 2018)

    Thermoreversible gelling polymer PF127 combined with other polymers

    Latanoprost

    Glaucoma

    In vitro, rabbit

    (Shastri et al., 2010)

    TS injectable CS/gelatin/glycerophosphate system

    In vitro

    (Cheng et al., 2014)

    TS crosslinked PNIPAAm hydrogels

    Rat

    (Turturro et al., 2011)

    NS, nanostructured; TS, thermosensitive, thermoresponsive; SS, stimuli sensitive; IS, ion sensitive; DR, dual responsive; CS, chitosan; AMD, DME, age-related macular degeneration and diabetic macular edema; PNIPAAm, poly(N-isopropylacrylamide); HSV, herpes simplex virus; CMV, cytomegalovirus; PLGA, poly(lactic-co-glycolic acid); PEG, poly(ethylene glycol).

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