The Immune System in Human Milk: A Historic Perspective

2.

Goldman

AS

,

Chheda

S

,

Keeney

SE

.

Immunology of human milk and host immunity

. In:

Polin

RL

,

Abman

S

,

Rowitch

DH

,

Benitz

W

, editors.

Fetal and neonatal physiology

. 6th ed.

Philadelphia (PA)

:

Elsevier

;

2021

.

https://doi.org/10.1089/bfm.2012.0025

3.

Goldman

AS

.

Evolution of immune functions of the mammary gland and protection of the infant

.

Breastfeed Med

.

2012

;

7

:

132

–

42

.

.

https://doi.org/10.1007/s10911-007-9051-7

4.

Wheeler

TT

,

Hodgkinson

AJ

,

Prosser

CG

,

Davis

SR

.

Immune components of colostrum and milk--a historical perspective

.

J Mammary Gland Biol Neoplasia

.

2007

;

12

:

237

–

47

.

.

5.

Diamantis

A

,

Magiokinis

E

,

Androustsos

G

.

Alfred François Donné (1801–1878)

.

J Med Biogr

.

2009

;

17

:

81

–

7

.

6.

Classics of science: the daguerreotype

.

The science news-letter

. 374th ed.

Society for Science & the Public

;

1928

.

Vol. 13

.

7.

Donné

A

.

Du Lait et en particulier de celui des Nourrices: considéré sous le rapport de ses bonnes et de ses mauvaises qualités nutritives et de altérations

.

Paris

:

Val. Repert. III

;

1837

.

8.

Donné

AF

.

Cours de microscopie

.

Paris

:

J.B. Bailliére

;

1845

.

https://doi.org/10.1203/00006450-196803000-00005

9.

Smith

CW

,

Goldman

AS

.

The cells of human colostrum. I. In vitro studies of morphology and functions

.

Pediatr Res

.

1968

;

2

:

103

–

9

.

.

https://doi.org/10.1002/cyto.990130310

10.

Wirt

DP

,

Adkins

LT

,

Palkowetz

KH

,

Schmalstieg

FC

,

Goldman

AS

.

Activated and memory T lymphocytes in human milk

.

Cytometry

.

1992

;

13

:

282

–

90

.

.

11.

Keeney

SE

,

Schmalstieg

FC

,

Palkowetz

KH

,

Rudloff

HE

,

Goldman

AS

.

Activated neutrophils and neutrophil activators in human milk. Increased expression of CD11b and decreased expression of L-selectin

.

J Leukocyte Biol

.

1993

;

54

:

97

–

104

.

https://doi.org/10.3945/an.114.006924

12.

Hassiotou

F

,

Hartmann

PE

.

At the dawn of a new discovery: the potential of breast milk stem cells

.

Adv Nutr

.

2014

;

5

:

770

–

8

.

.

https://doi.org/10.1258/jmb.2008.008006

13.

Schmalstieg

FC

Jr,

Goldman

AS

.

Ilya Ilich Metchnikoff (1845–1915) and Paul Ehrlich (1854–1915): the centennial of the 1908 nobel prize in physiology or medicine

.

J Med Biogr

.

2008

;

16

:

96

–

103

.

.

14.

Ehrlich

P

.

Experimentelle untersuchangen über immunität. I Über ricin

.

Dtsch Med Wochenschr

.

1891

;

17

:

976

–

9

.

15.

Ehrlich

P

,

Hubner

W

.

Experimentelle untersuchangen über immunität. II. Über abrin

.

Dtsch Med Wochenschr

.

1891

;

17

:

1218

–

9

.

https://doi.org/10.1159/000229177

16.

Hanson

LÅ

.

Comparative immunological studies of the immune globulins of human milk and of blood serum

.

Int Arch Allergy Appl Immunol

.

1961

;

18

:

241

–

67

.

.

17.

Ouchterlony

O

.

Antigen-antibody reactions in gels

.

Acta Pathol Microbiol Scand

.

1949

;

26

:

507

–

15

.

18.

Grabar

P

,

Williams

CA

Jr.

Méthode permettant l’étude conjugée des propriétés électrophorétiques et immunochemiques d’un mélange de proteins. Application au serum sanguine

.

Biochem Biophys Acta

.

1953

;

10

:

193

–

4

.

https://doi.org/%2010.1007/978-1-4020-8749-3_19

19.

Hanson

LA

.

Macy-György prize lecture: my milky way

.

Adv Exp Med Biol

.

2009

;

639

:

283

–

90

.

https://doi.org/10.1111/j.1365-3083.1978.tb00494.x

20.

Brandtzaeg

P

.

Polymeric IgA is complexed with secretory component (SC) on the surface of human intestinal epithelial cells

.

Scand J Immunol

.

1978

;

8

:

39

–

52

.

.

21.

Molé

CM

,

Montagne

PM

,

Béné

MC

,

Faure

GC

.

Sequential assay of human milk immunoglobulins shows a predominance of lambda chains

.

Lab Invest

.

1992

;

67

:

147

–

51

.

22.

Ahlstedt

S

,

Carlsson

B

,

Hanson

LÅ

,

Goldblum

RM

.

Antibody production by human colostral cells. I. Immunoglobulin class, specificity, and quantity

.

Scand J Immunol

.

1975

;

4

:

535

–

9

.

https://doi.org/10.1084/jem.146.5.1311

23.

Roux

ME

,

McWilliams

M

,

Phillips-Quagliata

JM

,

Weisz-Carrington

P

,

Lamm

ME

.

Origin of IgA-secreting plasma cells in the mammary gland

.

J Exp Med

.

1977

;

146

:

1311

–

22

.

.

https://doi.org/10.1016/s0022-3476(81)80447-7

24.

Fishaut

M

,

Murphy

D

,

Neifert

M

,

McIntosh

K

,

Ogra

PL

.

Bronchomammary axis in the immune response to respiratory syncytial virus

.

J Pediatr

.

1981

;

99

:

186

–

91

.

.

https://doi.org/10.1098/rspb.1922.0023

25.

Fleming

A

.

On a remarkable bacteriolytic element found in tissues and secretions

.

Proc R Soc Lond B

.

1922

;

93

(

653

):

306

.

.

26.

Fleming

A

,

Allison

VD

.

Observations on a bacteriolytic substance (“lysozyme”) found in secretions and tissues

.

Brit J Exp Path

.

1922

;

3

:

252

–

60

.

27.

Schmalstieg

FC

Jr,

Goldman

AS

.

Jules Bordet (1870–1961): a bridge between early and modern immunology

.

J Med Biogr

.

2009

;

17

:

217

–

24

.

28.

Bordet

J

,

Mordet

M

.

Le pouvoir bactériolytique du colostrum et du lait

.

Comptes Rendus des Séaces de L’Academie des Sciences

.

1924

;

179

:

1109

–

13

.

https://doi.org/10.1038/1921187b0

29.

Jollès

P

,

Jollès

J

.

Lysozyme from human milk

.

Nature

.

1961

;

192

(

4808

):

1187

–

8

.

.

30.

Sørensen

M

,

Sørensen

SPL

.

The proteins in whey

.

Comp rend des Travaux du Laboratoire de Carlsberg Série Chem

.

1939

;

23

:

55

–

90

.

https://doi.org/10.1038/143629a0

31.

Cosbie

AJC

.

Prof. S. P. L. Sørensen

.

Nature

.

1939

;

143

(

3624

):

629

.

.

32.

Schäfer

KH

.

Elektrophoretische untersuchungen zum milcheiweissproblem

.

Monatsschr Kinderheilkd

.

1951

;

99

:

69

–

71

.

https://doi.org/10.1021/ja01498a029

33.

Groves

ML

.

The isolation of a red protein from milk2

.

J Am Chem Soc

.

1960

;

82

(

13

):

3345

–

50

.

.

34.

Montreuil

J

,

Tonnelat

J

,

Mullet

S

.

Preparation and properties of lactosiderophilin (lactotransferrin) of human milk

.

Biochim Biophys

.

1960

;

45

:

413

–

21

.

35.

Blanc

B

,

Isliker

HC

.

Isolement et caractérisation de la protéine rouge sidérophile du lait maternal: la lactoferrine

.

Helv Physiol Pharmacol Acta

.

1961

;

19

:

C13

–

4

.

https://doi.org/10.3891/acta.chem.scand.23-0683

36.

Johansson

BG

.

Isolation of crystalline lactoferrin from human milk

.

Acta Chem Scand

.

1969

;

23

:

683

–

4

.

.

37.

Anderson

BF

,

Baker

HM

,

Dodson

EJ

,

Norris

GE

,

Rumball

SV

,

Waters

JM

, .

Structure of human lactoferrin at 3.2-Å resolution

.

Proc Natl Acad Sci U S A

.

1987

;

84

:

1769

–

73

.

https://doi.org/10.1016/s0022-3476(80)80676-7

38.

Fransson

GB

,

Lönnerdal

B

.

Iron in human milk

.

J Pediatr

.

1980

;

96

:

380

–

4

.

.

https://doi.org/10.1136/bmj.1.5792.69

39.

Bullen

JJ

,

Rogers

HJ

,

Leigh

L

.

Iron-binding proteins in milk and resistance to Escherichia coli infection in infants

.

Br Med J

.

1972

;

1

:

69

–

75

.

.

40.

Hâkansson

A

,

Svensson

M

,

Mossberg

AK

,

Sabharwal

H

,

Linse

S

,

Lazou

I

, .

A folding variant of alpha-lactalbumin with bactericidal activity against Streptococcus pneumoniae

.

Mol Microbiol

.

2000

;

35

:

589

–

600

.

https://doi.org/10.4049/jimmunol.170.3.1452

41.

Hieshima

K

,

Ohtani

H

,

Shibano

M

,

Izawa

D

,

Nakayama

T

,

Kawasaki

Y

, .

CCL28 has dual roles in mucosal immunity as a chemokine with broad-spectrum antimicrobial activity

.

J Immunol

.

2003

;

170

:

1452

–

61

.

.

https://doi.org/10.1128/iai.60.7.2893-2899.1992

42.

Schroten

H

,

Hanisch

FG

,

Plogmann

R

,

Hacker

J

,

Uhlenbruck

G

,

Nobis-Bosch

R

, .

Inhibition of adhesion of S-fimbriated Escherichia coli to buccal epithelial cells by human milk fat globule membrane components: a novel aspect of the protective function of mucins in the nonimmunoglobulin fraction

.

Infect Immun

.

1992

;

60

:

2893

–

9

.

.

https://doi.org/10.1203/00006450-199810000-00006

43.

Peterson

JA

,

Hamosh

M

,

Scallan

CD

,

Ceriani

RL

,

Henderson

TR

,

Mehta

NR

, .

Milk fat globule glycoproteins in human milk and in gastric aspirates of mother’s milk-fed preterm infants

.

Pediatr Res

.

1998

;

44

:

499

–

506

.

.

https://doi.org/10.4049/jimmunol.1201642

44.

Jaillon

S

,

Mancuso

G

,

Hamon

Y

,

Beauvillain

C

,

Cotici

V

,

Midiri

A

, .

Prototypic long pentraxin PTX3 is present in breast milk, spreads in tissues, and protects neonate mice from Pseudomonas aeruginosa lung infection

.

J Immunol

.

2013

;

191

:

1873

–

82

.

.

https://doi.org/10.1067/mpd.2001.109375

45.

Jia

HP

,

Starner

T

,

Ackermann

M

,

Kirby

P

,

Tack

BF

,

McCray

PB

.

Abundant human beta-defensin-1 expression in milk and mammary gland epithelium

.

J Pediatr

.

2001

;

138

:

109

–

12

.

.

https://doi.org/10.1093/glycob/cws074

46.

Bode

L

.

Human milk oligosaccharides: every baby needs a sugar mama

.

Glycobiology

.

2012

;

22

:

1147

–

62

.

.

47.

Farré-Maduell

E

,

Casals-Pascual

C

.

The origins of gut microbiome research in Europe: from Escherich to tissier

.

Hum Microbiome J

.

2019

;

14

:

100065

.

48.

Montreuil

J

,

Renner

B

,

Sawatzki

GG

.

The saga of human milk gynolactose, new perspectives in infant nutrition

.

Stuttgart (NY)

:

Georg Thieme Verlag

;

1992

.

https://doi.org/10.1016/0003-9861(54)90325-2

49.

György

P

,

Hoover

JR

,

Kuhn

R

,

Rose

CS

.

Bifidus factor. III. The rate of dialysis

.

Arch Biochem Biophys

.

1954

;

48

:

209

–

13

.

.

https://doi.org/10.1111/j.1651-2227.1986.tb10275.x

50.

Goldman

AS

,

Thorpe

LW

,

Goldblum

RM

,

Hanson

LA

.

Anti-inflammatory properties of human milk

.

Acta Paediatr Scand

.

1986

;

75

:

689

–

95

.

.

https://doi.org/10.1001/archpedi.1969.02100030144004

51.

Mata

LJ

,

Urrutia

JJ

,

García

B

,

Fernández

R

,

Béhar

M

.

Shigella infection in breast-fed Guatemalan Indian neonates

.

Am J Dis Child

.

1969

;

117

:

142

–

6

.

.

https://doi.org/10.1126/science.6968093

52.

Carpenter

G

.

Epidermal growth factor is a major growth-promoting agent in human milk

.

Science

.

1980

;

210

:

198

–

9

.

.

https://doi.org/10.1097/00005176-199201000-00010

53.

Buescher

ES

,

McIlheran

SM

.

Colostral antioxidants: separation and characterization of two activities in human colostrum

.

J Pediatr Gastroenterol Nutr

.

1992

;

14

:

47

–

56

.

.

54.

Kijlstra

A

,

Jeurissen

SH

.

Modulation of classical C3 convertase of complement by tear lactoferrin

.

Immunology

.

1982

;

47

:

263

–

70

.

https://doi.org/10.1203/00006450-198206000-00016

55.

Lindberg

T

,

Ohlsson

K

,

Weström

B

.

Protease inhibitors and their relation to protease activity in human milk

.

Pediatr Res

.

1982

;

16

:

479

–

83

.

.

https://doi.org/10.1111/1523-1747.ep12339292

56.

Park

PW

,

Biedermann

K

,

Mecham

L

,

Bissett

DL

,

Mecham

RP

.

Lysozyme binds to elastin and protects elastin from elastase-mediated degradation

.

J Invest Dermatol

.

1996

;

106

:

1075

–

80

.

.

https://doi.org/10.1179/096805102125001000

57.

Caccavo

D

,

Pellegrino

NM

,

Altamura

M

,

Rigon

A

,

Amati

L

,

Amoroso

A

, .

Antimicrobial and immunoregulatory functions of lactoferrin and its potential therapeutic application

.

J Endotoxin Res

.

2002

;

8

:

403

–

17

.

.

https://doi.org/10.1159/000243746

58.

Shimizu

T

,

Yamashiro

Y

,

Yabuta

K

.

Prostaglandin E1, E2, and F2 alpha in human milk and plasma

.

Biol Neonate

.

1992

;

61

:

222

–

5

.

.

https://doi.org/10.1016/s0022-2275(20)36953-4

59.

Furukawa

M

,

Narahara

H

,

Yasuda

K

,

Johnston

JM

.

Presence of platelet-activating factor-acetylhydrolase in milk

.

J Lipid Res

.

1993

;

34

:

1603

–

9

.

.

https://doi.org/10.1016/0090-6980(90)90030-y

60.

Caplan

M

,

Hsueh

W

,

Kelly

A

,

Donovan

M

.

Serum PAF acetylhydrolase increases during neonatal maturation

.

Prostaglandins

.

1990

;

39

:

705

–

14

.

.

https://doi.org/10.1097/00001648-199601000-00015

61.

Norris

JM

,

Scott

FW

.

A meta-analysis of infant diet and insulin-dependent diabetes mellitus: do biases play a role

.

Epidemiology

.

1996

;

7

:

87

–

92

.

.

https://doi.org/10.1001/jama.290.13.1721

62.

Ziegler

AG

,

Schmid

S

,

Huber

D

,

Hummel

M

,

Bonifacio

E

.

Early infant feeding and risk of developing type 1 diabetes-associated autoantibodies

.

JAMA

.

2003

;

290

:

1721

–

8

.

.

https://doi.org/10.1016/s0140-6736(88)92835-8

63.

Davis

MK

,

Savitz

DA

,

Graubard

BI

.

Infant feeding and childhood cancer

.

Lancet

.

1988

;

2

:

365

–

8

.

.

https://doi.org/10.1136/bmj.302.6792.1580

64.

Koletzko

S

,

Griffiths

A

,

Corey

M

,

Smith

C

,

Sherman

P

.

Infant feeding practices and ulcerative colitis in childhood

.

BMJ

.

1991

;

302

:

1580

–

1

.

.

https://doi.org/10.1136/bmj.298.6688.1617

65.

Koletzko

S

,

Sherman

P

,

Corey

M

,

Griffiths

A

,

Smith

C

.

Role of infant feeding practices in development of Crohn’s disease in childhood

.

BMJ

.

1989

;

298

:

1617

–

8

.

.

https://doi.org/10.1111/j.1651-2227.1984.tb09950.x

66.

Stephens

S

,

Kennedy

CR

,

Lakhani

PK

,

Brenner

MK

.

In-vivo immune responses of breast- and bottle-fed infants to tetanus toxoid antigen and to normal gut flora

.

Acta Paediatr Scand

.

1984

;

73

:

426

–

32

.

.

https://doi.org/10.1136/adc.61.3.263

67.

Stephens

S

.

Development of secretory immunity in breast fed and bottle fed infants

.

Arch Dis Child

.

1986

;

61

:

263

–

9

.

.

https://doi.org/10.1203/00006450-198902000-00021

68.

Goldblum

RM

,

Schanler

RJ

,

Garza

C

,

Goldman

AS

.

Human milk feeding enhances the urinary excretion of immunologic factors in low birth weight infants

.

Pediatr Res

.

1989

;

25

:

184

–

8

.

.

69.

Mellor

L

,

Miller

JFAP

.

Faculty of medicine online museum and archive

.

Australia

:

The University of Sydney

;

2008

.

https://doi.org/10.1098/rspb.1962.0048

70.

Miller

JFAP

.

Effect of neonatal thymectomy on the immunological responsiveness of the mouse

.

Proc R Soc Lond B

.

1962

;

156

(

964

):

415

–

28

.

.

https://doi.org/10.1007/s004310051258

71.

Hasselbalch

H

,

Engelmann

MD

,

Ersboll

AK

,

Jeppesen

DL

,

Fleischer-Michaelsen

K

.

Breast-feeding influences thymic size in late infancy

.

Eur J Pediatr

.

1999

;

158

:

964

–

7

.

.

https://doi.org/10.1093/ajcn/80.3.722

72.

Ngom

PT

,

Collinson

AC

,

Pido-Lopez

J

,

Henson

SM

,

Prentice

AM

,

Aspinall

R

.

Improved thymic function in exclusively breastfed infants is associated with higher interleukin 7 concentrations in their mothers’ breast milk

.

Am J Clin Nutr

.

2004

;

80

:

722

–

8

.

.

https://doi.org/10.1097/00005176-200009000-00017

73.

Field

CJ

,

Thomson

CA

,

Van Aerde

JE

,

Parrott

A

,

Euler

A

,

Lien

E

, .

Lower proportion of CD45R0+ cells and deficient interleukin-10 production by formula-fed infants, compared with human-fed, is corrected with supplementation of long-chain polyunsaturated fatty acids

.

J Pediatr Gastroenterol Nutr

.

2000

;

31

:

291

–

9

.

.

https://doi.org/10.1016/j.jpeds.2009.11.019

74.

Garofalo

R

.

Cytokines in human milk

.

J Pediatr

.

2010

;

156

:

S36

–

40

.

.

https://doi.org/10.1016/j.jpeds.2018.11.024

75.

Goldman

AS

.

Future research in the immune system of human milk

.

J Pediatr

.

2019

;

206

:

274

–

9

.

.

https://doi.org/10.1016/s0022-3476(73)80453-6

76.

Goldman

AS

,

Smith

CW

.

Host resistance factors in human milk

.

J Pediatr

.

1973

;

82

:

1082

–

90

.

.

77.

Goldman

AS

.

The immune system of human milk: antimicrobial, antiinflammatory, and immunomodulating properties

.

Pediatr Infect Dis J

.

1993

;

12

:

664

–

72

.

https://doi.org/10.1093/jn/135.5.1286

78.

Isaacs

CE

.

Human milk inactivates pathogens individually, additively, and synergistically

.

J Nutr

.

2005

;

135

:

1286

–

8

.

.

https://doi.org/10.1203/00006450-200205000-00013

79.

Magi

B

,

Ietta

F

,

Romagnoli

R

,

Liberatori

S

,

Pallini

V

,

Bini

L

, .

Presence of macrophage migration inhibitory factor in human milk: evidence in the aqueous phase and milk fat globules

.

Pediatr Res

.

2002

;

51

:

619

–

24

.

.

https://doi.org/10.1155/2019/4078671

80.

Cattaneo

C

,

Caramaschi

A

,

Uga

E

,

Braghin

M

,

Cosi

G

,

Peila

C

, .

Analysis of toll-like receptors in human milk: detection of membrane-bound and soluble forms

.

J Immunol Res

.

2019

;

2019

:

1

–

12

.

.

81.

Buesher

EWS

,

Malinowska

I

.

Soluble receptors and cytokine antagonists in human milk

.

Pediatr Res

.

1996

;

34

:

839

–

44

.

82.

Issacs

CE

,

Thormar

H

,

Pessolano

T

.

Membrane-disruptive effect of human milk: inactivation of enveloped viruses

.

J Infect Dis

.

1986

;

154

:

966

–

71

.